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Projection patterns of surviving neurons in the dorsal lateral geniculate nucleus following discrete lesions of striate cortex: Implications for residual vision
Abstract
In four monkeys with long-standing partial ablation of the striate cortex pellets of horseradish peroxidase were placed in either the striate cortex immediately adjacent to the ablation, or in the extrastriate cortex of the ventral prelunate gyrus, i.e. in visual area V4. We examined the dorsal lateral geniculate nucleus to see whether surviving neurons, within the region that shows retrograde degeneration as a result of the cortical lesion, project to remaining striate cortex and/or to extrastriate cortex. Neurons labelled from extrastriate cortex were found throughout the degenerated region, whereas neurons labelled from striate cortex were confined to the border between the normal and degenerated region of the nucleus. This shows that isolated neurons found within the degenerated region survive striate cortex damage because they project to an extrastriate visual area, and not because their terminals depart from the otherwise strict topographic representation of the lateral geniculate nucleus on to striate cortex.
... Interestingly, these extrastriate-projecting geniculocortical neurons are not evenly represented across the magnocellular, parvocellular, and koniocellular layers of the LGN. Most extrastriate-projecting geniculocortical neurons are found in the koniocellular layers (Bullier and Kennedy, 1983;Cowey and Stoerig, 1989;Rodman et al., 2001;Sincich et al., 2004). However, a recent study showed that following long-term V1 lesions, some MT-projecting geniculocortical neurons were found outside the koniocellular layers and expressed parvalbumin, a neurochemical marker for magnocellular and parvocellular LGN neurons, as well as calbindin, a marker for koniocellular neurons (Atapour et al., 2022). ...
... However, a recent study showed that following long-term V1 lesions, some MT-projecting geniculocortical neurons were found outside the koniocellular layers and expressed parvalbumin, a neurochemical marker for magnocellular and parvocellular LGN neurons, as well as calbindin, a marker for koniocellular neurons (Atapour et al., 2022). Surprisingly, while multiple studies have examined extrastriate-projecting geniculocortical neurons (Yukie and Iwai, 1981;Bullier and Kennedy, 1983;Cowey and Stoerig, 1989;Rodman et al., 2001;Sincich et al., 2004), none have investigated reciprocal, direct (i.e., V1-bypassing) corticogeniculate neurons in mid-level extrastriate cortex. The assumption being that corticogeniculate neurons, and corticothalamic neurons projecting to first-order thalamus in general, are present only in primary sensory cortices. ...
... Direct, V1-bypassing geniculocortical inputs to extrastriate visual cortex have been documented (Bullier and Kennedy, 1983;Cowey and Stoerig, 1989;Rodman et al., 2001;Sincich et al., 2004). However, reciprocal corticogeniculate circuits that similarly connect extrastriate visual cortex with the LGN directly, also bypassing V1, have never been confirmed using monosynaptic tracing methods (but see Lin and Kaas, 1977). ...
First-order thalamic nuclei receive feedforward signals from peripheral receptors and relay these signals to primary sensory cortex. Primary sensory cortex, in turn, provides reciprocal feedback to first-order thalamus. Because the vast majority of sensory thalamocortical inputs target primary sensory cortex, their complementary corticothalamic neurons are assumed to be similarly restricted to primary sensory cortex. We upend this assumption by characterizing morphologically diverse neurons in multiple mid-level visual cortical areas of the primate ( Macaca mulatta ) brain that provide direct feedback to the primary visual thalamus, the dorsal lateral geniculate nucleus (LGN). Although the majority of geniculocortical neurons project to primary visual cortex (V1), a minority, located mainly in the koniocellular LGN layers, provide direct input to extrastriate visual cortex. These “V1-bypassing” projections may be implicated in blindsight. We hypothesized that geniculocortical inputs directly targeting extrastriate cortex should be complemented by reciprocal corticogeniculate circuits. Using virus-mediated circuit tracing, we discovered corticogeniculate neurons throughout three mid-level extrastriate areas: MT, MST, and V4. Quantitative morphological analyses revealed nonuniform distributions of unique cell types across areas. Many extrastriate corticogeniculate neurons had spiny stellate morphology, suggesting possible targeting of koniocellular LGN layers. Importantly though, multiple morphological types were observed across areas. Such morphological diversity could suggest parallel streams of V1-bypassing corticogeniculate feedback at multiple stages of the visual processing hierarchy. Furthermore, the presence of corticogeniculate neurons across visual cortex necessitates a reevaluation of the LGN as a hub for visual information rather than a simple relay.
... However, a surviving population of LGN neurons retains visual function, including receptive fields inside the scotomas (6). At least some of these neurons receive retinal inputs (7) and form direct projections to extrastriate areas (3,8,9). This evidence is compatible with the hypothesis that surviving neurons within the LPZs provide one of the pathways for the mediation of residual visual function within the scotomas [blindsight (10)], as also indicated by functional studies in human and nonhuman primates (11-13). ...
... These lesions also trigger degenerative changes in the lateral geniculate nucleus (LGN) of the thalamus, which is the critical link between the retina and V1. Over several months, the majority of neurons in the affected sector of the LGN (lesion projection zone, LPZ) undergo retrograde degeneration leading to a marked reduction in the volume of this nucleus (2)(3)(4)(5). However, a surviving population of LGN neurons retains visual function, including receptive fields inside the scotomas (6). ...
... However, a surviving population of LGN neurons retains visual function, including receptive fields inside the scotomas (6). At least some of these neurons receive retinal inputs (7) and form direct projections to extrastriate areas (3,8,9). This evidence is compatible with the hypothesis that surviving neurons within the LPZs provide one of the pathways for the mediation of residual visual function within the scotomas [blindsight (10)], as also indicated by functional studies in human and nonhuman primates (11)(12)(13). ...
Significance
Lesions of the primary visual area (V1) in primates cause blindness by severing the main pathway which brings information from the thalamus to the cortex. However, some visual abilities remain, which are hypothesized to be mediated by thalamic neurons that innervate surviving areas such as the middle temporal (MT) cortex. We found that V1 lesions trigger long-term plasticity in the connections between the thalamus and cortex, including the emergence of a pathway that brings information to MT from cell populations that would normally project to V1. These results reveal potential targets for rehabilitation strategies to ameliorate the consequences of cortical blindness.
... Second, the projection from the inferior pulvinar to the extrastriate cortex also receives direct retinal, as well as retinotectal (superior colliculus), input. A third pathway, not illustrated, that potentially contributes consists of the parvocellular and magnocellular neurons that survive degeneration after area V1 injury, likely because they project directly to the extrastriate cortex (Cowey & Stoerig 1989 V1-bypassing pathways visually modulate area V2 and V3 in the absence of V1 input in the macaque. (a) Phase-encoding retinotopic map of a slice through the right posterior hemisphere of a macaque, whose V1 is intact. ...
... The most common cortical injury that leads to significant deficits in human patients involves V1 lesions (Bruce et al. 2006, Zhang et al. 2006, which are the most difficult to rehabilitate. This is compounded by the fact that following V1 lesions there is significant (>90% in the macaque) retrograde degeneration of the parvocellular and magnocellular pathways going back to the retina (Cowey & Stoerig 1989). It is likely that an even greater degree of retrograde degeneration occurs in the human (Polyak 1957), suggesting that perceptual aspects of vision are likely to be permanently and markedly changed post-V1 lesions, even under the best-case scenario of successful rehabilitation. ...
... However, all hope may not be lost. In the LGN, the koniocellular pathway survives, as well as scattered parvocellular and magnocellular neurons (perhaps as many as 10%), likely because they project directly to the extrastriate cortex (Cowey & Stoerig 1989, Sincich et al. 2004). This raises the possibility that, if strengthened appropriately, these surviving projections may mediate a degree of visual perception. ...
Much remains to be understood about visual system malfunction following injury. The resulting deficits range from dense, visual field scotomas to mild dysfunction of visual perception. Despite the predictive value of anatomical localization studies, much patient-to-patient variability remains regarding (a) perceptual abilities following injury and (b) the capacity of individual patients for visual rehabilitation. Visual field perimetry is used to characterize the visual field deficits that result from visual system injury. However, standard perimetry mapping does not always precisely correspond to underlying anatomical or functional deficits. Functional magnetic resonance imaging can be used to probe the function of surviving visual circuits, allowing us to classify better how the pattern of injury relates to residual visual perception. Identifying pathways that are potentially modifiable by training may guide the development of improved strategies for visual rehabilitation. This review discusses primary visual cortex lesions, which cause dense contralateral scotomas.
... The neurons incorporate the marker and transport it to their axonal termination. After appropriate delay (depends on the type of histological marker), the animal is sacrificed and histological sections of the brain are studied after specific histological staining [16]. Two categories of markers exist: anterograde and retrograde [21]. ...
... Cowey and Stoerig [16] studied the projection patterns of surviving neurons in the LGN following discrete lesions of V1 in macaques. Forty-eight hours after injecting horseradish peroxidase in V4, they realized histological sections of the occipital lobe and LGN. ...
... Histological marker axonal transportation studies in monkeys show markings in the sagittal stratum [16]. DTI studies realized by Bridge et al. [9] are in favor of a nondescribed sub-component of the sagittal stratum connecting LGN and V5/MT. ...
The aim of this paper is to review the literature on direct geniculo-extrastriate pathways with special attention to 3D extrastriate visual areas.
A literature review was realized using PubMed and Google Scholar. "Lateral geniculate nucleus", "geniculo-extrastriate pathways" and "white matter fiber tracts" were among the keywords used.
Existence of geniculo-extrastriate connections was first hypothesized by the clinical observations of Riddoch's syndrome in patients with striate cortex (primary visual area, V1) lesions. Robust histological proof of geniculo-extrastriate pathways exists in monkeys. In humans, these pathways were tested through functional magnetic resonance imaging (fMRI), electro- and magneto-physiological paradigms. Conversely, only indirect proof of the connection between lateral geniculate nucleus and V5 exists. To our knowledge there were not any anatomical studies of geniculo-extrastriate connections in humans.
Few human studies take interest in geniculo-extrastriate pathways. Only indirect proof of geniculo-extrastriate pathways exists in humans.
... Later anatomic studies have shown that some portion of the pulvinar directly receive the retinal inputs, which could convey the visual signal to the cerebral cortex (Kaas and Lyon, 2007;Gattass et al., 2014). In contrast, the direct route from the lateral geniculate nucleus (LGN) to the extrastriate cortex has been suggested to play a role in blindsight (Cowey and Stoerig, 1989). Schmid et al. (2010) showed that visual responses in the extrastriate visual areas disappeared after inactivation of the LGN during passive viewing after V1 lesioning in a macaque model. ...
... Both thalamic nuclei can send signals to the extrastriate cortex (Cowey and Stoerig, 1989;Hendry and Yoshioka, 1994;Berman and Wurtz, 2010). However, we cannot directly compare the roles of the LGN and pulvinar with these contradictory studies, because there are several critical differences among the subjects in these studies, such as the size of the lesion, the way the lesion was made, and the time after lesioning. ...
After damage to the primary visual cortex (V1), conscious vision is impaired. However, some patients can respond to visual stimuli presented in their lesion-affected visual field using residual visual pathways bypassing V1. This phenomenon is called “blindsight.” Many studies have tried to identify the brain regions responsible for blindsight, and the pulvinar and/or lateral geniculate nucleus (LGN) are suggested to play key roles as the thalamic relay of visual signals. However, there are critical problems regarding these preceding studies in that subjects with different sized lesions and periods of time after lesioning were investigated; furthermore, the ability of blindsight was assessed with different measures. In this study, we used double dissociation to clarify the roles of the pulvinar and LGN by pharmacological inactivation of each region and investigated the effects in a simple task with visually guided saccades (VGSs) using monkeys with a unilateral V1 lesion, by which nearly all of the contralesional visual field was affected. Inactivating either the ipsilesional pulvinar or LGN impaired VGS toward a visual stimulus in the affected field. In contrast, inactivation of the contralesional pulvinar had no clear effect, but inactivation of the contralesional LGN impaired VGS to the intact visual field. These results suggest that the pulvinar and LGN play key roles in performing the simple VGS task after V1 lesioning, and that the visuomotor functions of blindsight monkeys were supported by plastic changes in the visual pathway involving the pulvinar, which emerged after V1 lesioning.
... This result is not surprising considering the main role of both structures in visual signal transmission. The LGN is the primary relay of visual signal to V1. Destruction of V1 in primates yields extensive retrograde degeneration of LGN (Cowey & Stoerig, 1989;Hendrickson et al., 2015), with near complete loss of P and M cells (Mihailovic, Cupic, & Dekleva, 1971), leading to 'cortical blindness' (Brindley, Gautier-Smith, & Lewin, 1969;Stoerig, Zontanou, & Cowey, 2002). On the other hand, pulvinar, along with only the K layers of LGN, are implicated in residual visual capacity following damage to V1 because they project directly to extrastriate cortex (Cowey & Stoerig, 1989;Cowey, Stoerig, & Bannister, 1994). ...
... The LGN is the primary relay of visual signal to V1. Destruction of V1 in primates yields extensive retrograde degeneration of LGN (Cowey & Stoerig, 1989;Hendrickson et al., 2015), with near complete loss of P and M cells (Mihailovic, Cupic, & Dekleva, 1971), leading to 'cortical blindness' (Brindley, Gautier-Smith, & Lewin, 1969;Stoerig, Zontanou, & Cowey, 2002). On the other hand, pulvinar, along with only the K layers of LGN, are implicated in residual visual capacity following damage to V1 because they project directly to extrastriate cortex (Cowey & Stoerig, 1989;Cowey, Stoerig, & Bannister, 1994). ...
Traditionally, the dorsal lateral geniculate nucleus (LGN) and the inferior pulvinar (IPul) nucleus are considered as anatomically and functionally distinct thalamic nuclei. However, in several primate species it has also been established that the koniocellular (K) layers of LGN and parts of the IPul have a shared pattern of immunoreactivity for the calcium‐binding protein calbindin. These calbindin‐rich cells constitute a thalamic matrix system which is implicated in thalamocortical synchronization. Further, the K layers and IPul are both involved in visual processing and have similar connections with retina and superior colliculus. Here we confirmed the continuity between calbindin‐rich cells in LGN K layers and the central lateral division of IPul (IPulCL) in marmoset monkeys. By employing a high‐throughput neuronal tracing method, we found that both the K layers and IPulCL form comparable patterns of connections with striate and extrastriate cortices; these connections are largely different to those of the parvocellular and magnocellular laminae of LGN. Retrograde tracer‐labeled cells and anterograde tracer‐labeled axon terminals merged seamlessly from IPulCL into LGN K layers. These results support continuity between LGN K layers and IPulCL, providing an anatomical basis for functional congruity of this region of the dorsal thalamic matrix, and calling into question the traditional segregation between LGN and the inferior pulvinar nucleus. This article is protected by copyright. All rights reserved.
... HVFs repeated without intervening training revealed decreases in both local and overall (PMD) sensitivity. Whether this represents a form of visual disuse atrophy, a consequence of retrograde degeneration of neurons in the dorsal lateral geniculate nucleus (dLGN) and retina, [27][28][29][30][31] or whether patients learned to ignore weak, unreliable vision near their blind field remains to be determined. That worsening was not systematically reported previously may be due to HVF analyses in prior studies lacking sensitivity to such changes. ...
... While speculative, a possible substrate of traininginduced visual improvements in CB is engagement of extrageniculostriate pathways. Projections from the dLGN that bypass V1 provide direct input to V2/ V3, 34-36 V4, 29 and MT/MST. 37 These pathways may mediate blindsight 38 -residual visual processing present in some CB fields. ...
Objective:
To assess if visual discrimination training improves performance on visual perimetry tests in chronic stroke patients with visual cortex involvement.
Methods:
24-2 and 10-2 Humphrey visual fields were analyzed for 17 chronic cortically blind stroke patients prior to and following visual discrimination training, as well as in 5 untrained, cortically blind controls. Trained patients practiced direction discrimination, orientation discrimination, or both, at nonoverlapping, blind field locations. All pretraining and posttraining discrimination performance and Humphrey fields were collected with online eye tracking, ensuring gaze-contingent stimulus presentation.
Results:
Trained patients recovered ∼108 degrees(2) of vision on average, while untrained patients spontaneously improved over an area of ∼16 degrees(2). Improvement was not affected by patient age, time since lesion, size of initial deficit, or training type, but was proportional to the amount of training performed. Untrained patients counterbalanced their improvements with worsening of sensitivity over ∼9 degrees(2) of their visual field. Worsening was minimal in trained patients. Finally, although discrimination performance improved at all trained locations, changes in Humphrey sensitivity occurred both within trained regions and beyond, extending over a larger area along the blind field border.
Conclusions:
In adults with chronic cortical visual impairment, the blind field border appears to have enhanced plastic potential, which can be recruited by gaze-controlled visual discrimination training to expand the visible field. Our findings underscore a critical need for future studies to measure the effects of vision restoration approaches on perimetry in larger cohorts of patients.
... One such pathway projects from the retina to the koniocellular (intercalated) layers of the lateral geniculate nucleus directly, or to the superior colliculus and from there to extrastriate cortex. This pathway originates in the retinal Pγ class of ganglion cells, which comprises ~10% of the total ganglion cell number is particularly dense near the fovea (Henry and Reid, 2000), and is known to survive retrograde degeneration following V1 lesions (Cowey and Stoerig, 1989). Another V1-bypassing pathway projects from the retina to the pulvinar directly or via the superior colliculus and from there to the extrastriate visual areas. ...
... Two pathways stand out as potentially mediating the residual activity observed in extrastriate cortex , as well as related aspects of blindsight behavior: 1) The koniocellular pathway (dotted lines) from the K (intercalated) layers of the thalamus directly to areas V2, V3, V4, V5/MT. This pathway originates in the retinal Pγ class of ganglion cells, comprising ~10% of total ganglion cells, survives retrograde degeneration following V1 lesions, and is particularly dense near the fovea (Cowey and Stoerig, 1989;Henry and Reid, 2000). This pathway receives both direct retinal and superior collicular input. ...
Partial damage of the primary visual cortex (V1) and optic radiation lesions can cause visual eld de cits restricted to speci c regions of the contralateral visual hemi eld. This thesis has explored the functional properties of the visual cortex and its capacity to reorganize in patients with chronic V1 or optic radiation lesions resulting in partial or complete homonymous quadrantanopia. We used functional magnetic resonance (fMRI) methods and quantitative population receptive eld (pRF) analysis to investigate: i) how spared regions of the visual cortex cover the visual eld following V1 injury, and ii) whether the retinotopic organization of the spared visual cortex changes as a result of reorganization. We demonstrate that the spared part of area V1 has at best a limited-degree of reorganization that manifests in some patients with a small shift of the pRF centers towards the border of the scotoma and by a slight increase in V1 pRF sizes near the border of the scotoma. Importantly, we show that responses in early and higher visual cortex are not always congruent with visual perception in subjects with visual cortical lesions. Several patterns of mismatch were identi ed: 1) visual eld areas covered in both areas V1 and hV5/MT+, 2) visual eld areas covered in hV5/MT+ but not V1 suggesting the existence of functional pathways that bypass area V1. Interestingly these areas overlap with dense regions of the perimetric scotoma, suggesting that activity in these areas does not contribute to visual awareness. Nevertheless, identifying and characterizing the patterns of activation seen in the visual cortex may help choose visual eld locations with high potential for rehabilitation. Conversely, we found cases in which 3) spared area V1 failed to cover completely seeing visual eld locations in the perimetric map, suggesting the existence of V1-bypassing pathways that are able to mediate useful vision. Understanding how the properties of visual areas change after injury, and how this correlates with perception is important in the e ort to adopt new rational strategies for visual rehabilitation. Finally, we reviewed the literature and proposed a systematic approach to visual system rehabilitation using the combination of pRF mapping and real-time fMRI neuro-feedback methods.
... One such pathway projects from the retina to the koniocellular (intercalated) layers of the lateral geniculate nucleus directly, or to the superior colliculus and from there to extrastriate cortex. This pathway originates in the retinal Pγ class of ganglion cells, which comprises ~10% of the total ganglion cell number is particularly dense near the fovea (Henry and Reid, 2000), and is known to survive retrograde degeneration following V1 lesions (Cowey and Stoerig, 1989). Another V1-bypassing pathway projects from the retina to the pulvinar directly or via the superior colliculus and from there to the extrastriate visual areas. ...
... Two pathways stand out as potentially mediating the residual activity observed in extrastriate cortex (Rodman et al., 1989;Schmid et al., 2009;Schmid et al., 2010), as well as related aspects of blindsight behavior: 1) The koniocellular pathway (dotted lines) from the K (intercalated) layers of the thalamus directly to areas V2, V3, V4, V5/MT. This pathway originates in the retinal Pγ class of ganglion cells, comprising ~10% of total ganglion cells, survives retrograde degeneration following V1 lesions, and is particularly dense near the fovea (Cowey and Stoerig, 1989;Henry and Reid, 2000). This pathway receives both direct retinal and superior collicular input. ...
To date, we have little understanding of how the visual cortex reorganizes after injury, and no proven effective treatment strategies to rehabilitate the recovery of visual perception in the affected portion of the visual field in V1-lesioned patients. Understanding how to manipulate the brain’s capacity for plasticity is an important step in the long-term effort to design treatments aiming to enhance the ability of the nervous system to recover after injury. To make progress along this front, we need to: i) study the mechanisms by which the adult brain adapts and reorganizes after injury; and ii) devise approaches that will allow us to manipulate the process of reorganization to induce visual recovery.
... The visual projections that are not destined for V1 arise from two principal sources, namely the dorsal lateral geniculate nucleus and the pulvinar via the superior colliculus. Using anatomical staining techniques, direct projections from the dorsal lateral geniculate nucleus to prestriate areas have been shown to target V2, V3 and V4 (Benevento and Yoshida, 1981; Yukie and Iwai, 1981; Stoerig and Cowey, 1989). The projections via the superior colliculus exhibit cone input, and spectral opponency is observed in the pulvinar (Felsten et al., 1983), so some P-type projection to subcortical structures is likely. ...
... Thus, patients are little affected when their discriminations are made on the basis of transience or motion, which are stimulus attributes encoded by the M-type system (Merigan et al., 1991) and probably areas in the dorsal stream, in particular V5 (Zeki, 1978; Newsome and Pare, 1988). Poor colour responses would be expected on the basis of weak input to ventral pathways (Yukie and Iwai, 1981) and fewer than normal P-type projections following V1 lesion (Cowey et al., 1989). The lack of highresolution receptive field properties in the superior colliculus (Goldberg and Wurtz, 1972) and prestriate areas (Zeki, 1993) is also consistent with the severely affected spatial responses in patients. ...
... Goebel, Muckli, Zanella, Singer, & Stoerig, 2001;Rodman, Gross, & Albright, 1989a;Schmid, Panagiotaropoulos, Augath, Logothetis, & Smirnakis, 2009), and these activations are functionally significant, as their disruption by transcranial magnetic stimulation (TMS) impairs blindsight performance (Alexander & Cowey, 2009). Blindsight is likely to be mediated by pathways projecting directly to extrastriate cortex, bypassing V1 (Cowey & Stoerig, 1989;Rodman, Gross, & Albright, 1989b;Schmid et al., 2010). ...
... However, this possibility is ruled out by demonstrations of subcortical pathways which can activate extrastriate areas in the absence of V1 (e.g. Rodman et al., 1989aRodman et al., , 1989bCowey & Stoerig, 1989;Goebel et al., 2001;Schmid et al., 2010) and by brain stimulation evidence indicating that these extrastriate activations are necessary for blindsight (Alexander & Cowey, 2009). Thus in the absence of V1, the argument goes, extrastriate regions can be activated and this activation can guide visual functions but not reach conscious experience. ...
The neuropsychological phenomenon of blindsight has been taken to suggest that the primary visual cortex (V1) plays a unique role in visual awareness, and that extrastriate activation needs to be fed back to V1 in order for the content of that activation to be consciously perceived. The aim of this review is to evaluate this theoretical framework and to revisit its key tenets. Firstly, is blindsight truly a dissociation of awareness and visual detection? Secondly, is there sufficient evidence to rule out the possibility that the loss of awareness resulting from a V1 lesion simply reflects reduced extrastriate responsiveness, rather than a unique role of V1 in conscious experience? Evaluation of these arguments and the empirical evidence leads to the conclusion that the loss of phenomenal awareness in blindsight may not be due to feedback activity in V1 being the hallmark awareness. On the basis of existing literature, an alternative explanation of blindsight is proposed. In this view, visual awareness is a "global" cognitive function as its hallmark is the availability of information to a large number of perceptual and cognitive systems; this requires inter-areal long-range synchronous oscillatory activity. For these oscillations to arise, a specific temporal profile of neuronal activity is required, which is established through recurrent feedback activity involving V1 and the extrastriate cortex. When V1 is lesioned, the loss of recurrent activity prevents inter-areal networks on the basis of oscillatory activity. However, as limited amount of input can reach extrastriate cortex and some extrastriate neuronal selectivity is preserved, computations involving comparison of neural firing rates within a cortical area remain possible. This enables "local" read-out from specific brain regions, allowing for the detection and discrimination of basic visual attributes. Thus blindsight is blind due to lack of "global" long-range synchrony, and it functions via "local" neural readout from extrastriate areas.
... following a V1 lesion and suggested its critical role in enabling residual visual capacity. Despite severe retrograde degeneration of the LGN following a visual cortex lesion (Hendrickson et al., 2015), a small population of cells residing in the K layers survived and maintained a projection to MT (Figure 20.3B) (Cowey and Stoerig, 1989;Sincich et al., 2004). This projection was con rmed in human blindsight patients (Ajina and Bridge, 2018), forming the modern-day LGN hypothesis of blindsight. ...
The Cerebral Cortex and Thalamus is guided by two central and related tenets, the thalamus plays an ongoing and essential role in cortical functioning, and the cortex is essential for thalamic functioning. Accordingly, neither the cortex nor the thalamus can be understood in any meaningful way in the absence of the other. With chapters written by more than 100 leading experts in the field, The Cerebral Cortex and Thalamus provides a comprehensive account of the structure, function, development, and evolution of the circuitry interconnecting the thalamus and cortex and the consequences of pathology on these circuits.
... Lesions in the primary visual cortex (V1) trigger degeneration and volume loss in the lateral geniculate nucleus (LGN), both in human and non-human primates (Atapour et al., 2017Cowey & Stoerig, 1989;Hendrickson et al., 2015;Simmen et al., 2022). The widespread degeneration involves projection neurons in the magno-(M), parvo (P), and koniocellular (K) neurons as well as corticogeniculate fibers (Atapour et al., 2017;Kinoshita et al., 2019;Wong-Riley, 1972). ...
Lesions of the primary visual cortex (V1) cause retrograde neuronal degeneration, volume loss and neurochemical changes in the lateral geniculate nucleus (LGN). Here we characterise the timing of these processes, by comparing the LGN of adult marmoset monkeys following various recovery times after unilateral V1 lesions. Observations in NeuN-stained sections obtained from animals with very short (3 days) recoveries showed that the volume and neuronal density in the LGN ipsilateral to the lesions were similar to those in the contralateral hemispheres. However, neuronal density in the LGN lesion projection zones (LPZ) dropped rapidly thereafter, with a loss of ~50% of the population occurring within a month of the lesions. This level of neuronal loss was then sustained for the remainder of the range of recovery times, up to >3 years post-lesion. In comparison, shrinkage of the LGN progressed more gradually, not reaching a stable value until 6 months post lesion. We also determined the time course of the expression of the calcium-binding protein calbindin (CB) in magnocellular (M) and parvocellular (P) layer neurons, a recently described form of neurochemical plasticity triggered by V1 lesions. We found that CB expression could be detected in surviving M and P neurons as early as 1 month after a lesion, with the percentage of neurons showing this neurochemical phenotype showing subtle changes over 6 months. Our study shows that there is a limited time window for any possible interventions aimed at reducing secondary neuronal loss in the visual afferent pathways following damage to V1.
... Additionally, the SC-LGN pathway has been shown to survive transneuronal retrograde degeneration following V1 lesions (although not a glaucoma model). 56 The existence of an SC-pulvinar-V5/MT pathway has also been suggested, 57,58 as well as direct projections of the LGN to V5/MT. 59,60 Therefore, the SC is proposed to take over V1ʹs role via the pulvinar or LGN in these cases. ...
Glaucoma is a common condition that relies on careful clinical assessment to diagnose and determine disease progression. There is growing evidence that glaucoma is associated not only with loss of retinal ganglion cells but also with degeneration of cortical and subcortical brain structures associated with vision and eye movements. The effect of glaucoma pathophysiology on eye move- ments is not well understood. In this review, we examine the evidence surrounding altered eye movements in glaucoma patients compared to healthy controls, with a focus on quantitative eye tracking studies measuring saccades, fixation, and optokinetic nystagmus in a range of visual tasks. The evidence suggests that glaucoma patients have alterations in several eye movement domains. Patients exhibit longer saccade latencies, which worsen with increasing glaucoma severity. Other saccadic abnormalities include lower saccade amplitude and velocity, and difficulty inhibiting reflexive saccades. Fixation is pathologically altered in glaucoma with reduced stability. Optokinetic nystagmus measures have also been shown to be abnormal. Complex visual tasks (eg reading, driving, and navigating obstacles), integrate these eye movements and result in behavioral adaptations. The review concludes with a summary of the evidence and recommendations for future research in this emerging field.
... Involvement of ipsilesional IPS area in visuomotor function after V1 lesion suggested by PET imaging was supported by unit recordings, where ipsilesional lbIPS neurons showed clear phasic visual responses similarly to contralesional/intact lbIPS neurons. As for the thalamic relay of visual information to the cortex, the pulvinar [30][31][32][33] , and/or the lateral geniculate nucleus [34][35][36] are considered to contribute to blindsight, presumably depending on the properties of visual signals to be processed, as proposed by Tamietto and Morrone 37 . Area MT is thought to receive visual inputs from these subcortical areas 31,35 and provide visual information to the lbIPS and MST regions in blindsight; thus, it is reasonable that we observed a cluster in the ipsilesional IPS/MT/ MST regions in our imaging results. ...
Patients with damage to the primary visual cortex (V1) lose visual awareness, yet retain the ability to perform visuomotor tasks, which is called “blindsight.” To understand the neural mechanisms underlying this residual visuomotor function, we studied a non-human primate model of blindsight with a unilateral lesion of V1 using various oculomotor tasks. Functional brain imaging by positron emission tomography showed a significant change after V1 lesion in saccade-related visuomotor activity in the intraparietal sulcus area in the ipsi- and contralesional posterior parietal cortex. Single unit recordings in the lateral bank of the intraparietal sulcus (lbIPS) showed visual responses to targets in the contralateral visual field on both hemispheres. Injection of muscimol into the ipsi- or contralesional lbIPSs significantly impaired saccades to targets in the V1 lesion-affected visual field, differently from previous reports in intact animals. These results indicate that the bilateral lbIPSs contribute to visuomotor function in blindsight.
... Retrograde (presynaptic) degeneration of retinal ganglion cells and retinal nerve fibers following damage to the occipital lobe has been documented extensively (Beatty, Sadun, Smith, Vonsattel, & Richardson, 1982;Cowey & Stoerig, 1989;Dinkin, 2017). ...
Macular degeneration (MD) is a common visual disorder in the aging population characterized by a loss of central vision, reduced visual acuity contrast sensitivity, and increased crowding. This impairment strongly affects the quality of life and personal autonomy. There is currently no cure for AMD, available treatment options are only able to slow down the disease, and even palliative treatments are rare. After the emergence of the central scotoma, patients with MD develop one or more eccentric fixation areas - preferred retinal loci (PRLs) - that are used for fixation, reading, tracking, and other visual tasks that require finer ocular abilities. The final goal of the project was to investigate and to improve the residual visual abilities in the PRL. Four studies were conducted in total. Study 1 was conducted in MD patients to investigate whether after the emergence of the scotoma, the PRL acquire enhanced abilities in the processing of the visual information through spontaneous or use-dependent adaptive plasticity. Study 2 aimed to assess the effects of a single administration of transcranial random noise electrical stimulation (tRNS), a subtype of non-invasive transcranial electrical stimulation, on the spatial integration in the healthy visual cortex. Study 3 aimed to assess the between session effect of daily repeated tRNS coupled with perceptual training. The objective of study 4 was to translate the previous findings into a clinically applicable treatment approach by combining tRNS and perceptual training in adult patients with MD. Contrary to previous results, we found neither a phenomenon of spontaneous nor use-dependent cortical plasticity undergoing in the PRL before the training. We also found that the tRNS was able to modulate the visuospatial integration in the early visual processing, promoting plastic changes in the stimulated network. Its effects were not limited to the short-term modulation but also produced a boosting of the learning in a crowding task. The final experiment showed that a combination of tRNS and perceptual training could result in greater improvements and larger transfer to untrained visual tasks in adults with MD than training alone. Overall, our results indicate that tRNS of the visual cortex has potential application as an additional therapy to improve vision in adults with bilateral central blindness.
... The most consistently reported projection arises from koniocellular cells, present mostly within the K or interlaminar layers of the LGN, which projects to area MT (Stepniewska et al., 2000;Sincich et al., 2004;Dick et al., 1991;Warner et al., 2010). There are, however, additional reports of connections between the LGN and other extrastriate visual areas, such as the second visual area (V2; Benevento and Yoshida, 1981;Fries, 1981;Bullier and Kennedy, 1983), fourth visual area (V4; Lysakowski et al., 1988;Tanaka et al., 1990;Cowey and Stoerig, 1989;Lyon and Rabideau, 2012), and the inferior temporal area (Yukie and Iwai, 1981) in macaque monkeys, as well as area 19 in marmosets (Dick et al., 1991) or the dorsal medial area in prosimian galagos and owl monkeys (Beck and Kaas, 1998). Connections between the LGN and these additional extrastriate areas have not been Figure 4 Extent of both striate (V1; dark blue) and extrastriate cortical areas (light blue), in the rat (A), squirrel (B), tree shrew (C), galago (D), marmoset (E), squirrel monkey (F), and macaque monkey (G). ...
There are multiple routes for visual information to reach the neocortex from the retina. The most well studied are those that pass through the lateral geniculate nucleus of the thalamus and arrive at cortex primarily within V1. From V1, visual information is then disseminated onto extrastriate cortical visual areas. However, there are other less well-studied pathways that bypass V1 and directly target extrastriate visual fields. These include pathways that route through the K layers of the lateral geniculate nucleus or the pulvinar, either by direct or indirect retinal input via the superior colliculus. The focus of this chapter is on these alternative visual pathways that project to extrastriate cortical areas, our current understanding of their possible evolution by reviewing comparative data across primates and their close relatives, and the insights these pathways could provide in our understanding of visual perception in the normal and injured brain.
... For a long time, the LGN route appeared an unlikely candidate due to strong degeneration caused by V1 injury. But evidence in macaques shows that a significant amount of cells projecting directly towards visual association cortex survive this degeneration [9,43]. Pharmacological inactivation of LGN neurons eliminated functional activation of visual association cortex and visual detection capacities in a monkey model of blindsight [44] ( Figure 2b). ...
Vision rests on computations that primarily rely on the parvo- and magnocellular geniculate relay of retinal signals to V1. Secondary pathways involving superior colliculus, koniocellular lateral geniculate nucleus and pulvinar and their V1-bypassing projections to higher order cortex are known to exist. While they may form an evolutionary old visual system, their contribution to perception and visually guided behaviour remain largely obscure. Recent developments in tract tracing and circuit manipulation technologies provide new insights. Here we discuss how secondary visual pathways mediate residual vision (blindsight) after V1 injury by relaying signals directly into higher order cortical areas. We contrast these findings on blindsight with new studies on dyslexia suggesting that dysfunction of secondary visual pathways might contribute to dyslexic's perceptual difficulties. Emerging from these considerations, secondary visual pathways involving koniocellular LGN may be critical for detection of visual change, whereas pulvinar function appears more linked to visuomotor planning.
... However, as to the role of Pul, Kaas and colleagues suggested that it should be minimal, because the tecto-recipient zone of the Pul minimally overlaps the areas with the area containing the neurons projecting to the extrastriate cortex 12 . On the other hand, Cowey and Stoerig 13 showed that there are surviving neurons in the dorsal lateral geniculate nucleus (dLGN), which project to the extrastriate cortex, after the V1 lesion and suggested that they would mediate the visual inputs directly to the extrastriate cortex in blindsight monkeys. It was later shown that a part of koniocellular layer neurons (K-cells) in the dLGN 14 directly project to the area middle temporal area (MT) 15 . ...
In patients with damage to the primary visual cortex (V1), residual vision can guide goal-directed movements to targets in the blind field without awareness. This phenomenon has been termed blindsight, and its neural mechanisms are controversial. There should be visual pathways to the higher visual cortices bypassing V1, however some literature propose that the signal is mediated by the superior colliculus (SC) and pulvinar, while others claim the dorsal lateral geniculate nucleus (dLGN) transmits the signal. Here, we directly test the role of SC to ventrolateral pulvinar (vlPul) pathway in blindsight monkeys. Pharmacological inactivation of vlPul impairs visually guided saccades (VGS) in the blind field. Selective and reversible blockade of the SC-vlPul pathway by combining two viral vectors also impairs VGS. With these results we claim the SC-vlPul pathway contributes to blindsight. The discrepancy would be due to the extent of retrograde degeneration of dLGN and task used for assessment.
... The LGN is often implicated in blindsight as a possible nonstriate source of input to the extrastriate cortex [3,37,38]. Neuroanatomical studies suggest that there is a direct connection between the LGN and extrastriate cortex [39,40], including specific projections to middle temporal area (MT) [41][42][43]. However, its relatively small size and deep location makes it particularly challenging to image [44]. ...
Author summary
When the primary visual cortex (V1) is damaged in one hemisphere, we lose the ability to see one half of the world around us. Clinical tests show that in this blind region of vision, we cannot see even the brightest flashes of light. However, many years of research have shown that individuals who are blind in this way may still respond to certain images in the ‘blind’ area of vision, even though they are often unable to describe what they ‘see’ and may be unaware of seeing anything at all. This is called blindsight, and researchers are trying to understand the pathways underlying this phenomenon. A recent study mapped a physical pathway of connections in the brain that could account for blindsight in humans. However, the functional nature of this pathway has never been shown. In this study, we assess a group of patients with damage to V1, some of whom demonstrate blindsight and some of whom do not. We compare neural responses and functional connectivity and show that a functional connection in this pathway is critical for blindsight. We also reveal new insights into how speed and motion are likely to be processed in the healthy brain.
... The most consistently reported projection arises from koniocellular cells, present mostly within the K or interlaminar layers of the LGN, which projects to area MT (Stepniewska et al., 2000;Sincich et al., 2004;Dick et al., 1991;Warner et al., 2010). There are, however, additional reports of connections between the LGN and other extrastriate visual areas, such as the second visual area (V2; Benevento and Yoshida, 1981;Fries, 1981;Bullier and Kennedy, 1983), fourth visual area (V4; Lysakowski et al., 1988;Tanaka et al., 1990;Cowey and Stoerig, 1989;Lyon and Rabideau, 2012), and the inferior temporal area (Yukie and Iwai, 1981) in macaque monkeys, as well as area 19 in marmosets (Dick et al., 1991) or the dorsal medial area in prosimian galagos and owl monkeys (Beck and Kaas, 1998). Connections between the LGN and these additional extrastriate areas have not been Figure 4 Extent of both striate (V1; dark blue) and extrastriate cortical areas (light blue), in the rat (A), squirrel (B), tree shrew (C), galago (D), marmoset (E), squirrel monkey (F), and macaque monkey (G). ...
There are multiple routes for visual information to reach the neocortex from the retina. The most well studied are those that pass through the lateral geniculate nucleus of the thalamus and arrive at cortex primarily within V1. From V1, visual information is then disseminated onto extrastriate cortical visual areas. However, there are other less well-studied pathways that bypass V1 and directly target extrastriate visual fields. These include pathways that route through the K layers of the lateral geniculate nucleus or the pulvinar, either by direct or indirect retinal input via the superior colliculus. The focus of this chapter is on these alternative visual pathways that project to extrastriate cortical areas, our current understanding of their possible evolution by reviewing comparative data across primates and their close relatives, and the insights these pathways could provide in our understanding of visual perception in the normal and injured brain.
... Primary sensory and motor regions are "special" within the array of areas, having unique recognition mecha nisms and extremely strong trophic dependence in development on their specific t halamic input nucleus. For example, the lateral geniculate nucleus of the thalamus, relaying visual information from the retina, will project only to primary visual cortex, and the thalamus must make that connection for its neurons to survive ( Mihailović et al. 1971;Wong-Riley 1972;Cowey and Stoerig 1989). The primary sensory and motor areas serve to anchor the other areas in the cortical sheet and anchor its a nterior-to-posterior polarity. ...
This chapter discusses some features of mammalian brain development that similarly confer computational, and hence behavioral, robustness and evolvability at multiple scales with a focus on the isocortex. It focuses particularly on standing gradients of neuronal proliferation that cause the isocortex to scale over six orders of magnitude in volume, yet reliably produces species-specific capacities like whisker grooming or tool-making, nocturnal or diurnal vision, echolocation or language. The chapter specifies the computational organization entailed by the well known association of brain size with behavioral complexity, so that one might begin to reify the nature of processing speed and computational capacity. It also discusses the scaling and functional consequences of an anterior-posterior gradient of neurogenesis across the developing isocortex. The chapter argues that an increase in cortex volume is not an indeterminate addition of neurons, but a particular, progressive amplification of a hierarchically organized information-processing strategy.
... La mise en jeu d'autres voies de traitement de l'information visuelle pourrait également expliquer la rapidité avec laquelle le système visuel est capable de catégoriser des stimuli. Il existe, par exemple, des projections du CGL qui atteignent directement le cortex extra-strié, en court-circuitant l'aire V1 (Cowey and Stoerig 1989;Fries 1981;Girard and Bullier 1989;Hernandez-Gonzalez, Cavada et al. 1994;Yukie and Iwai 1988). On observe également qu'une partie des axones de cellules ganglionnaires ne rejoint pas le CGL et projette sur le colliculus supérieur, formant ainsi la voie visuelle rétino-tectale. ...
L’expression faciale de peur constitue un important vecteur d’information sociale mais aussi
environnementale. En condition naturelle, les visages apeurés apparaissent principalement
dans notre champ visuel périphérique. Cependant, les mécanismes cérébraux qui sous-tendent
la perception de l’expression faciale de peur en périphérie restent largement méconnus. Nous
avons démontré, grâce à des études comportementales, des enregistrements
magnétoencéphalographiques et intracrâniens, que la perception de l’expression faciale de
peur est efficace en grande périphérie. La perception de la peur en périphérie génère une
réponse rapide de l’amygdale et du cortex frontal, mais également une réponse plus tardive
dans les aires visuelles occipitales et temporales ventrales. Le contrôle attentionnel est capable
d’inhiber la réponse précoce à l’expression de peur, mais également d’augmenter les activités
postérieures plus tardives liées à la perception des visages. Nos résultats montrent non
seulement que les réseaux impliquées dans la perception de la peur sont adaptés à la vision
périphrique, mais ils mettent également en avant une nouvelle forme d’investigation des
mécanismes de traitement de l’expression faciale, pouvant conduire à une meilleure
compréhension des mécanismes de traitement des messages sociaux dans des situations plus
écologiques.
... This finding corroborates the hypothesis that hMT/V5 may receive information through a direct pathway from the LGN. Indeed, one of the two dominant views has suggested that neurons from the LGN may project directly to extrastriate visual cortex, possibly from intralaminar k-cells, allowing information to be processed independently of V1 (Cowey and Stoerig, 1989;Schmid et al., 2010). Alternatively, a second influential view suggests that a subcortical pathway to the SC and pulvinar, and from there to the extrastriate region may be the most likely route allowing V1-independent processing to take place (Rodman et al., 1990;Kato et al., 2011). ...
Fast and automatic behavioral responses are required to avoid collision with an approaching stimulus. Accordingly, looming stimuli have been found to be highly salient and efficient attractors of attention due to the implication of potential collision and potential threat. Here, we address the question of whether looming motion is processed in the absence of any functional primary visual cortex and consequently without awareness. For this, we investigated a patient (TN) suffering from complete, bilateral damage to his primary visual cortex. Using an fMRI paradigm, we measured TN's brain activation during the presentation of looming, receding, rotating, and static point lights, of which he was unaware. When contrasted with other conditions, looming was found to produce bilateral activation of the middle temporal areas, as well as the superior temporal sulcus and inferior parietal lobe (IPL). The latter are generally thought to be involved in multisensory processing of motion in extrapersonal space, as well as attentional capture and saliency. No activity was found close to the lesioned V1 area. This demonstrates that looming motion is processed in the absence of awareness through direct subcortical projections to areas involved in multisensory processing of motion and saliency that bypass V1.
... La mise en jeu d'autres voies de traitement de l'information visuelle pourrait également expliquer la rapidité avec laquelle le système visuel est capable de catégoriser des stimuli. Il existe, par exemple, des projections du CGL qui atteignent directement le cortex extra-strié, en court-circuitant l'aire V1 (Cowey and Stoerig 1989;Fries 1981;Girard and Bullier 1989;Hernandez-Gonzalez, Cavada et al. 1994;Yukie and Iwai 1988). On observe également qu'une partie des axones de cellules ganglionnaires ne rejoint pas le CGL et projette sur le colliculus supérieur, formant ainsi la voie visuelle rétino-tectale. ...
Facial expression of fear is an important vector of social and environmental information. In natural conditions, the frightened faces appear mainly in our peripheral visual field. However, the brain mechanisms underlying perception of fear in the periphery remain largely unknown. We have demonstrated, through behavioral, magnetoencephalographic and intracranial studies that the perception of fear facial expression is efficient in large peripheral visual field. Fear perception in the periphery produces an early response in the amygdala and the frontal cortex, and a later response in the occipital and infero-temporal visual areas. Attentional control is able to inhibit the early response to fear expression and to increase the later temporo-occipital activities linked to face perception. Our results show that networks involved in fear perception are adapted to the peripheral vision. Moreover, they validate a new form of investigation of facial expression processing, which may lead to a better understanding of how we process social messages in more ecological situations.
... However, there are also direct projections from the dorsolateral geniculate nucleus to extrastriate areas V2 (Hendry and Reid, 2000), MT (Sincich et al., 2004) and V4 (Cowey and Stoerig, 1989). These pathways are smaller than the main pathway from dorsolateral geniculate nucleus to V1, but recent evidence shows that inactivating the dorsolateral geniculate nucleus also decreases visually evoked responses in extrastriate visual areas (including V2, V3, V4 and MT) that remain active after V1 lesions in monkeys (Schmid et al., 2010). ...
Brain responses (from functional magnetic resonance imaging) and components of information processing were investigated in nine cortically blind observers performing a global direction discrimination task. Three of these subjects had responses in perilesional cortex in response to blind field stimulation, whereas the others did not. We used the EZ-diffusion model of decision making to understand how cortically blind subjects make a perceptual decision on stimuli presented within their blind field. We found that these subjects had slower accumulation of information in their blind fields as compared with their good fields and to intact controls. Within cortically blind subjects, activity in perilesional tissue, V3A and hMT+ was associated with a faster accumulation of information for deciding direction of motion of stimuli presented in the blind field. This result suggests that the rate of information accumulation is a critical factor in the degree of impairment in cortical blindness and varies greatly among affected individuals. Retraining paradigms that seek to restore visual functions might benefit from focusing on increasing the rate of information accumulation.
The primary visual cortex (V1) is one of the most studied regions of the brain and is characterized by its specialized and laminated layer 4 in human and non-human primates. However, studies aiming to harmonize the definition of the cortical layers and borders of V1 across rodents and primates are very limited. This article attempts to identify and harmonize the molecular markers and connectional patterns that can consistently link corresponding cortical layers of V1 and borders across mammalian species and ages. V1 in primates has at least two additional and unique layers (L3b2 and L3c) and two sublayers of layer 4 (L4a and L4b) compared to rodent V1. In all species examined, layers 4 and 3b of V1 receive strong inputs from the (dorsal) lateral geniculate nucleus, and V1 is mostly surrounded by the secondary visual cortex except for one location where V1 directly abuts area prostriata. The borders of primate V1 can also be clearly identified at mid-gestational ages using gene markers. In rodents, a novel posteromedial extension of V1 is identified, which expresses V1 marker genes and receives strong inputs from the lateral geniculate nucleus. This V1 extension was labeled as the posterior retrosplenial cortex and medial secondary visual cortex in the literature and brain atlases. Layer 6 of the rodent and primate V1 originates corticothalamic projections to the lateral geniculate, lateral dorsal, and reticular thalamic nuclei and the lateroposterior–pulvinar complex with topographic organization. Finally, the direct geniculo-extrastriate (particularly the strong geniculo-prostriata) projections are probably major contributors to blindsight after V1 lesions. Taken together, compared to rodents, primates, and humans, V1 has at least two unique middle layers, while other layers are comparable across species and display conserved molecular markers and similar connections with the visual thalamus with only subtle differences.
Background:
Cortical blindness is a form of severe vision loss that is caused by damage to the primary visual cortex (V1) or its afferents. This condition has devastating effects on quality of life and independence. While there are few treatments currently available, accumulating evidence shows that certain visual functions can be restored with appropriate perceptual training: Stimulus sensitivity can be increased within portions of the blind visual field. However, this increased sensitivity often remains highly specific to the trained stimulus, limiting the overall improvement in visual function.
Objective:
Recent advances in the field of perceptual learning show that such specificity can be overcome with training paradigms that leverage the properties of higher-level visual cortical structures, which have greater capacity to generalize across stimulus positions and features. This targeting can be accomplished by using more complex training stimuli that elicit robust responses in these visual structures.
Methods:
We trained cortically blind subjects with a complex optic flow motion stimulus that was presented in a location of their blind field. Participants were instructed to train with the stimulus at home for approximately 30 minutes per day. Once performance plateaued, the stimulus was moved deeper into the blind field. A battery of pre- and post-training measures, with careful eye tracking, was performed to quantify the improvements.
Results:
We show that 1) optic flow motion discrimination can be relearned in cortically blind fields; 2) training with an optic flow stimulus can lead to improvements that transfer to different tasks and untrained locations; and 3) such training leads to a significant expansion of the visual field. The observed expansion of the visual field was present even when eye movements were carefully controlled. Finally, we show that regular training is critical for improved visual function, as sporadic training reduced the benefits of training, even when the total numbers of training sessions were equated.
Conclusions:
These findings are consistent with the hypothesis that complex training stimuli can improve outcomes in cortical blindness, provided that patients adhere to a regular training regimen. Nevertheless, such interventions remain limited in their ability to restore functional vision.
In man and monkey, absolute cortical blindness is caused by destruction of the optic radiations and/or the primary visual cortex. It is characterized by an absence of any conscious vision, but stimuli presented inside its borders may nevertheless be processed. This unconscious vision includes neuroendocrine, reflexive, indirect and forced-choice responses which are mediated by the visual subsystems that escape the direct cerebral damage and the Ensuring degeneration. While extrastriate cortical areas participate in the mediation of the forced-choice responses, a concomitant striate cortical activation does not seem to be necessary for blindsight. Whether the loss of phenomenal vision is a necessary consequence of striate cortical destruction and whether this structure is indispensable for conscious sight are much debated questions which need to be tackled experimentally.
This chapter finally presents a characterization of interdisciplinary evolution of the machine brain. Perspective schemes for rebuilding a real vision brain in the future are analyzed, along with the major principles to construct the machine brain, are presented, which include memory, thinking, imagination, feeling, speaking and other aspects associated with machine vision, machine touch and machine minds. This explicitly developed the theoretical framework of brain-inspired intelligence from the vision brain hypothesis, the vision-minds hypothesis and the skin brain hypothesis. Based on Chaps. 2– 5, development of machine intelligence during the past decades have experienced three stages—machine computation, learning and understanding. Machine leaning includes data mining. Environmental sensing helps to acquire the data. Pattern analysis and scene understanding are significant parts of machine understanding. Scientists have taught machine how to collect and treat data and discover knowledge from the data. Evolution of machine brain will experience another two stages—machine meta-learning (learning to learn) and self-directed development (improving the capability of machine brain utilizing the learned knowledge). There are still great challenges in realization of the dream.
Alan Cowey's primary interest was in the way in which we interpret the visual world. This led him to study not only the early visual areas but also the inferotemporal and parietal cortex with which they are connected and the further projections into the eye field in the prefrontal cortex. His research interests were wide, covering colour vision, attention, visual neglect and the anatomical basis of the visual abilities that can be spared after a lesion in the primary visual cortex. Alan spent over 40 years at the University of Oxford, where he was involved in many initiatives and served on many committees, playing many important roles in the development of neuroscience as an interdisciplinary field of research.
Lesions of striate cortex (V1) trigger massive retrograde degeneration of neurons in the LGN. In primates, these lesions also lead to scotomas, within which conscious vision is abolished. Mediation of residual visual capacity within these regions (blindsight) has been traditionally attributed to an indirect visual pathway to the extrastriate cortex, which involves the superior colliculus and pulvinar complex. However, recent studies have suggested that preservation of the LGN is critical for behavioral evidence of blindsight, raising the question of what type of visual information is channeled by remaining neurons in this structure. A possible contribution of LGN neurons to blindsight is predicated on two conditions: that the neurons that survive degeneration remain visually responsive, and that their receptive fields continue to represent the region of the visual field inside the scotoma. We tested these conditions in male and female marmoset monkeys (Callithrix jacchus) with partial V1 lesions at three developmental stages (early postnatal life, young adulthood, old age), followed by long recovery periods. In all cases, recordings from the degenerated LGN revealed neurons with well-formed receptive fields throughout the scotoma. The responses were consistent and robust, and followed the expected eye dominance and retinotopy observed in the normal LGN. The responses had short latencies and preceded those of neurons recorded in the extrastriate middle temporal area. These findings suggest that the pathway that links LGN neurons to the extrastriate cortex is physiologically viable and can support residual vision in animals with V1 lesions incurred at various ages.
Stereoscopic vision (3D vision) is the ability to analyze the volume and the distance of the object (depth perception). Due to the important development of 3D cinemas and games, this ability is becoming increasingly important. We identified the visual cortical areas implicated in stereoscopic vision in a previous functional MRI study. Visual information processing is complex and only partially understood. Among the visual processing streams, only the optic radiations (geniculo-striate or geniculo-calcarine pathway) has been the subject of anatomical and functional studies. We have studied the connections between the stereoscopic visual areas. Connections between the lateral geniculate nucleus and some stereoscopic visual areas (IPS, V5) have been identified in diffusion tractography MRI.
During the past two decades, a myriad of studies have suggested a central pathogenic role for a-synuclein in Parkinson's disease. Recent studies have unravelled self-aggregation and prion-like spreading properties for a-synuclein. Of particular importance was the seminal observation of Lewy body-like structures in graftedfœtal dopaminergic neurons of patients with Parkinson's disease. This conceptual breakthrough generated the " host-to-the-graft " hypothesis or prion-like hypothesis. Nowadays, mechanisms underlying these new properties appear as putative disease-modifying targets. As the lack of valid animal models for Parkinson's disease is considered as a roadblock toward therapeutic intervention, the use of the newly developed models based on the prion-like properties of a-synuclein should allow future target validation.
Clinical neurologists have long known that some recovery of function after damage to the brain and spinal cord is possible, but the specific mechanisms mediating the process are still not completely understood. Part of the difficulty in defining the mechanisms of functional recovery stems from the fact that there may be multiple pathways leading to recovery. This is because brain and spinal cord injuries at the cellular and morphological level are not the result of a single causative event. Rather, they derive from an initial and relatively rapid biochemical cascade that then produces secondary cellular events leading to further destruction of nerve tissue. Many of the destructive events such as the breakdown of the blood—brain barrier, the excessive release of glutamate and other excitatory amino acids, dramatic changes in the levels of neurotransmitters such as gamma-aminobutyric acid (GABA) and norepinephrine, the production of oxygen free radicals, the release of arachidonic acid, lipid membrane peroxidation, and so forth are at the heart of much of the current research being conducted in university laboratories and pharmaceutical companies.
The lesion, which is usually a surgical ablation in monkey and vascular, traumatic, or neoplastic damage in man, destroys the striate cortical input to subcortical nuclei such as the superior colliculus and the pulvinar. It also causes retrograde degeneration of the ipsilateral geniculate nucleus (dLGN), which loses approximately 99% of its projection neurons in just a few months. Transneuronally, via the dLGN, the degeneration affects the retinal ganglion cell layer. Anatomical, physiological, and neuropsychological results show that the blindness caused by a striate cortical lesion is very different from that caused by corresponding retinal lesions. Sensitivity may be reduced by no more than half a log unit and performance may be 100% correct in a motion or color discrimination task. In spite of this high sensitivity and excellent performance, the patients do not perceive the stimuli they are reacting to.
The main purpose of this article is to review the most relevant results about relations between attention and visual awareness. More specifically, we examine classic and more recent work related with actual theories about the attentional mechanism. We also review the main results about the relevance of conscious processing and the work centred on the neural correlates of visual awareness. Most prominent models about the role of attention and consciousness are also considered. In sum, all this sort of evidence clearly shows that attentional networks are specifically implicated in different levels of consciousness.
Because of its distinctive architecture, connections, and functions, primary visual cortex, area 17 or V1 of primates, can be easily identified in most mammals (Kaas, 1987). V1 (also referred to as striate cortex) is particularly distinctive in primates, and, as a result, it was the first cortical area identified histologically (see Gennari, 1782, in Fulton, 1937). V1 of most, if not all, primates has a number of conspicuous features that distinguish this structure from its homologue in other mammals. Unlike carnivores, such as cats and ferrets, almost all of the visual input relayed from the lateral geniculate nucleus (LGN) of primates terminates in V1 (Benevento and Standage, 1982; Bullier and Kennedy, 1983; see Henry, 1991, for review), and lesions of V1 produce a severe deficit known as cortical blindness (e.g., Cowey and Stoerig, 1989). In addition, visual cortex of all primates is activated by physiologically and morphologically distinguishable streams, or channels, of inputs that are relayed from the retina to V1 in a manner unique to primates (Kaas and Huerta, 1988; Casagrande and Norton, 1991). Furthermore, the intrinsic connections of V1 in primates exhibit both vertical (laminar) and areal (modular) distinctions that appear designed to create new output channels from input channels via features of internal circuitry. Finally, the output streams project to visual areas that seem to be organized in a manner unique to primates. In particular, the major cortical target of V1, the second visual area, V2, is composed of three morphologically distinct modules that are differentially activated from V1, and at least one other major target of V1, the middle temporal visual area or MT, appears to be a unique specialization of primates (Kaas and Preuss, 1993). These common features of visual cortex in primates are of particular interest because these specializations relate to vision in humans as well as other primates. In this review, we focus on common features that have been described for V1 across a variety of primate species, and therefore are most likely to be present in most or all primates. In addition, we describe differences in V1 organization across primate groups, since these differences may relate to functional specializations and adaptations in the greatly varied primate order. Features that vary across taxa, when related to behavioral niches, may provide clues as to the significance of variations. Finally, this review briefly compares V1 in primates with V1 in some nonprimates to emphasize the distinctiveness of V1 in primates.
The extrastriate visual cortex of the monkey has in recent decades come to include an ever-expanding portion of the neocortical domain as more and more traditional “association” or even motor territories are shown to have significant visual connections, visual responsiveness, or role in visual behavior (Felleman and van Essen, 1991; also see the chapter by Gross in this volume). In this chapter, discussion will be restricted (or broadened, depending upon one’s viewpoint) to consideration of cortical zones shown to have at least some visual sensory responsiveness and direct connectivity with other, unimodal visual areas. First, we will consider the normal anatomical, physiological, and metabolic development of extrastriate visual cortex, including the prenatal specification of visual areas. Next, we will discuss the plasticity of extrastriate visual cortex in adulthood by examining the ability of extrastriate areas to function in parallel with striate cortex and the consequences of damage to extrastriate cortex in adult monkeys. In addition, we will examine evidence for learning-or experience-dependent plasticity in the response properties of neurons in extrastriate cortex. In the subsequent section, we will address the special plasticity associated with damage to visual cortex in developing animals. We will then briefly compare the development and plasticity of extratriate cortex in monkeys with phenomena described for other mammalian groups. In the final section, we will summarize the data presented and comment on general principles of extrastriate and cerebral cortical development.
The incidence of cortically induced blindness is increasing as our population ages. The major cause of cortically induced blindness is stroke affecting the primary visual cortex. While the impact of this form of vision loss is devastating to quality of life, the development of principled, effective rehabilitation strategies for this condition lags far behind those used to treat motor stroke victims. Here we summarize recent developments in the still emerging field of visual restitution therapy, and compare the relative effectiveness of different approaches. We also draw insights into the properties of recovered vision, its limitations and likely neural substrates. We hope that these insights will guide future research and bring us closer to the goal of providing much-needed rehabilitation solutions for this patient population.
This chapter summarizes the characteristics of cat ganglion cells that are vulnerable and those that appear to be largely insensitive to the cortical lesion. It reviews the relevant features of retinal ganglion structure, function, contributions to vision, and connectivity and also describes the impact of primary visual cortex lesions on ganglion cells and visually guided behavior. The elimination of β (X) cells has a potentially profound impact on visual processing in addition to the absence of primary visual cortex. The three most significant factors linked to the survival, and death of cat retinal ganglion cells following lesions of primary visual cortex are maturational status, patterns of connectivity, and rate of degeneration of lateral geniculate nucleus (LGN) neurons. β (X)-retinal ganglion cells in the cat and monkey, and by extension humans, have a unique and a signature array of morphological, physiological, and connectional characteristics that set them apart from all other ganglion cell types. They are also extremely fragile and depend for survival on primary visual cortex and its intermediate relay structure, the LGN, both some distance apart.
Maintaining or modifying the speed and direction of locomotion requires the coupling of the locomotion with the retinal optic flow that it generates. It is shown that this essential behavioral capability, which requires on-line neural control, is preserved in the cortically blind hemifield of a hemianope. In experiments, optic flow stimuli were presented to either the normal or blind hemifield while the patient was walking on a treadmill. Little difference was found between the hemifields with respect to the coupling (i.e. co-dependency) of optic flow detection with locomotion. Even in the cortically blind hemifield, faster walking resulted in the perceptual slowing of detected optic flow, and self-selected locomotion speeds demonstrated behavioral discrimination between different optic flow speeds. The results indicate that the processing of optic flow, and thereby on-line visuo-locomotor coupling, can take place along neural pathways that function without processing in Area V1, and thus in the absence of conscious intervention. These and earlier findings suggest that optic flow and object motion are processed in parallel along with correlated non-visual locomotion signals. Extrastriate interactions may be responsible for discounting the optical effects of locomotion on the perceived direction of object motion, and maintaining visually guided self-motion.
The superior colliculus (SC) is thought to be unresponsive to stimuli that activate only short wavelength-sensitive cones (S-cones) in the retina. The apparent lack of S-cone input to the SC was recognized by Sumner et al. [Sumner, P., Adamjee, T., & Mollon, J. D. Signals invisible to the collicular and magnocellular pathways can capture visual attention. Current Biology, 12, 1312-1316, 2002] as an opportunity to test SC function. The idea is that visual behavior dependent on the SC should be impaired when S-cone stimuli are used because they are invisible to the SC. The SC plays a critical role in blindsight. If the SC is insensitive to S-cone stimuli blindsight behavior should be impaired when S-cone stimuli are used. Many clinical and behavioral studies have been based on the assumption that S-cone-specific stimuli do not activate neurons in the SC. Our goal was to test whether single neurons in macaque SC respond to stimuli that activate only S-cones. Stimuli were calibrated psychophysically in each animal and at each individual spatial location used in experimental testing [Hall, N. J., & Colby, C. L. Psychophysical definition of S-cone stimuli in the macaque. Journal of Vision, 13, 2013]. We recorded from 178 visually responsive neurons in two awake, behaving rhesus monkeys. Contrary to the prevailing view, we found that nearly all SC neurons can be activated by S-cone-specific visual stimuli. Most of these neurons were sensitive to the degree of S-cone contrast. Of 178 visual SC neurons, 155 (87%) had stronger responses to a high than to a low S-cone contrast. Many of these neurons' responses (56/178 or 31%) significantly distinguished between the high and low S-cone contrast stimuli. The latency and amplitude of responses depended on S-cone contrast. These findings indicate that stimuli that activate only S-cones cannot be used to diagnose collicular mediation.
Visual learning has been intensively studied in higher mammals, both during development and in adulthood. What is less clear is the extent and properties such plasticity may acquire following permanent damage to the adult visual system. Answering this question is important. Aside from improving our understanding of visual processing in the absence of an intact visual circuitry, such knowledge is essential for the development of effective therapies to rehabilitate the increasing number of people who suffer the functional consequences of damage at different levels of their visual cortical hierarchy. This review summarizes the known characteristics of visual learning after adult visual cortex damage and begins to dissect some of the neural correlates of this process.
First published in 1995, this book presents a model for understanding the visual processing underlying perception and action, proposing a broad distinction within the brain between two kinds of vision: conscious perception and unconscious 'online' vision. It argues that each kind of vision can occur quasi-independently of the other, and is separately handled by a quite different processing system. For this new edition, the text from the original edition has been left untouched, standing as a coherent statement of the authors' position. However, a very substantial epilogue has been added to the book, which reviews some of the key developments that support or challenge the views that were put forward in the first edition. The new chapter summarizes developments in various relevant areas of psychology, neuroscience, and behaviour. It supplements the main text by updating the reader on the contributions that have emerged from the use of functional neuroimaging, which was in its infancy when the first edition was written. Neuroimaging, and functional MRI in particular, has revolutionized the field by allowing investigators to plot in detail the patterns of activity within the visual brains of behaving and perceiving humans. The authors show how its use now allows scientists to test and confirm their proposals, based largely on evidence accrued from primate neuroscience in conjunction with studies of neurological patients.
Although most projection neurons in the primate dorsal lateral geniculate nucleus (dLGN) target striate cortex (V1), a small number project instead to extrastriate visual areas and have been suggested to play a role in the preserved vision ("blindsight") that survives damage to V1. Moreover, the distribution of dLGN cells projecting to extrastriate bears a striking similarity to that of neurons that stain for calbindin D-28K (Cal), a calcium-binding protein involved in regulating neuronal excitability and considered a marker for the koniocellular or "K" pathway of geniculocortical processing. In these studies, we used double-labeling techniques to examine whether Cal content characterizes all or a subset of neurons making up the geniculo-extrastriate pathway in normal macaque monkeys. After injections of cholera toxin B-subunit into the prelunate gyrus, the proportion of retrogradely labeled neurons in the dLGN that were also immunoreactive for Cal varied from less than 40% to over 80%, indicating that only a subset of the geniculo-extrastriate projection falls within the K pathway as defined by Cal content. Analysis of the injected territories indicated that identity of the extrastriate cortical target may be systematically related to Cal content in the geniculo-extrastriate projection. To see whether the Cal-immunoreactive dLGN population might potentially play a role in preserved vision after V1 damage, we also examined the dLGN of a macaque that had sustained a lesion of V1 in infancy and survived until 4 years. In this animal, large, intensely Cal-immunoreactive neurons were found scattered throughout the otherwise degenerated dLGN zones and made up over 95% of the identifiable remaining neurons. The results support an emerging view that the macaque koniocellular system is highly heterogeneous in nature and also suggest that Cal content may be a critical feature of the pathway by which visual information reaches extrastriate cortex in the absence of V1.
Previous transneuronal anterograde tracing studies have shown that the retino-thalamic pathway to the posteromedial lateral suprasylvian (PMLS) visual area of cortex is heavier than normal in adult cats that received neonatal damage to visual cortical areas 17, 18, and 19. In contrast, the strength of this projection does not appear to differ from that in normal animals in cats that experienced visual cortex damage as adults. In the present study, we used retrograde tracing methods to identify the thalamic cells that project to the PMLS cortex in adult cats that had received a lesion of visual cortex during infancy or adulthood. In five kittens, a unilateral visual cortex lesion was made on the day of birth, and horseradish peroxidase (HRP) was injected into the PMLS cortex of both hemispheres when the animals were 10.5 to 13 months old. For comparison, HRP was injected bilaterally into the PMLS cortex of three cats 6.5 to 13.5 months after they received a similar unilateral visual cortex lesion as adults. In cats with a neonatal lesion, retrograde labeling was found in the large neurons that survive in the otherwise degenerated layers A and A1 of the lateral geniculate nucleus (LGN) ipsilateral to the lesion. Retrograde labeling of A-layer neurons was not seen in the undamaged hemisphere of these animals or in either hemisphere of animals that had received a lesion as adults. As in normal adult cats, retrograde labeling also was present in the C layers of the LGN, the medial interlaminar nucleus, the posterior nucleus of Rioch, the lateral posterior nucleus, and the pulvinar nucleus ipsilateral to a neonatal or adult lesion. Quantitative estimates indicate that the number of labeled cells is much larger than normal in the C layers of the LGN ipsilateral to a neonatal visual cortex lesion. Thus the results indicate that the heavier than normal projection from the thalamus to PMLS cortex that exists in adult cats after neonatal visual cortex damage arises, at least in part, from surviving LGN neurons in the A and C layers of the LGN. Although several thalamic nuclei, as well as the C layers of the LGN, continue to project to PMLS cortex after an adult visual cortex lesion, these projections appear not to be affected significantly by the lesion.
The dorsomedial visual area (DM) of owl monkeys is a cortical area that has been described recently in a range of primate species. To study the thalamic connections of this area, injections of several distinguishable neuroanatomical tracers were placed into DM in galagos, owl monkeys, squirrel monkeys, and macaque monkeys. The distribution of label was remarkably consistent across these diverse primate species. Labeled connections were densest within the pulvinar complex. Both the lateral and inferior divisions of the pulvinar, but not the medial division, had connections with DM. Within the inferior pulvinar of monkeys, central lateral and central medial nuclei had dense connections, and the medial and posterior nuclei had sparse connections with DM. Sparser connections were revealed in the lateral geniculate nucleus and the nucleus limitans. Anterograde label was also found in the superior colliculus. The consistencies in the pattern of subcortical projections across prosimian primates, New World monkeys, and Old World monkeys support the concept that DM is a visual area common to all primates. In addition, these results provide further evidence for proposed subdivisions of the inferior pulvinar. J. Comp. Neurol. 396:381–398, 1998. © 1998 Wiley-Liss, Inc.
In order to determine the relationship of superior colliculus inputs to thalamic neurons projecting to the middle temporal visual area (MT), injections of wheat germ agglutinin conjugated with horseradish peroxidase were placed in the superior colliculus of three owl monkeys, with injections of Fast Blue in the MT. The locations of labelled terminals and neurons in the posterior thalamus were related to four architectonically distinct nuclei of the inferior pulvinar (Stepniewska & Kaas, Vis. Neurosci.14, pp.1043–1060, 1997). Fast Blue injections in the MT labelled neurons largely in the medial nucleus of the inferior pulvinar. A few labelled neurons were found in the adjoining central medial nucleus of the inferior pulvinar, as well as in the lateral pulvinar and the dorsal lateral geniculate nucleus. Superior colliculus inputs were most dense in the posterior and medial nuclei of the inferior pulvinar. There were sparser inputs to the central lateral nucleus of the inferior pulvinar, locations in the lateral and medial pulvinar, and the dorsal lateral geniculate nucleus. The results indicate that the medial nucleus of the inferior pulvinar, the major projection zone to the MT, does not receive a significant input from the superior colliculus.
The middle temporal area (MT) of the macaque monkey is a region of extrastriate cortex involved in the analysis of visual motion. MT receives strong projections from striate cortex and from area V2, which is dependent on striate for visual responsiveness. Accordingly, the visual properties of MT neurons have been thought to reflect the further processing of its input from striate cortex. We examined the dependence of MT activity on pathways deriving from striate cortex by recording from MT neurons following removal of their striate input. Repeated recordings in area MT were made in 4 hemispheres of anesthetized macaques following either partial or total ablations of striate cortex. Cells in MT were tested for responsiveness, selectivity for direction of motion and direction tuning, and ocular dominance. Receptive fields were also plotted. In an additional animal, we recorded from MT neurons during reversible cooling of the central representation in striate cortex. We found that striate cortex removal or inactivation did not abolish the visual responsiveness of the majority of MT cells. Although the residual responses were generally much weaker than in the intact animal, direction selectivity and binocularity were still present. Moreover, receptive field size and overall topography appeared unaltered.
Cortical visual area V4 in macaque monkeys has a large proportion of neurons that are sensitive to the wavelength or to the color of light. We tested its role in hue discrimination by removing it in macaque monkeys trained to discriminate small differences in hue. Hue discrimination thresholds were permanently elevated in 4 macaque monkeys in which V4 was removed bilaterally. In contrast, there was no impairment in achromatic intensity thresholds tested in an identical manner. However, the discrimination of pattern and orientation was also conspicuously impaired, indicating that area V4 is not concerned solely with processing information about wavelength. The multiple defect is consistent with evidence that V4 provides the major cortical visual input to the temporal lobe, where a large range of visual properties is registered. The performance of monkeys with V4 ablation was compared with that of unoperated control monkeys and monkeys with removal of cortex in the banks and floor of the rostral superior temporal sulcus (STS). Removal of STS had only slight effects on pattern discrimination and none of hue discrimination. To control for the possible effects of inadvertent damage to the visual radiations when removing V4, the lateral striate cortex was partially ablated bilaterally in a control monkey. This had no effect on any discrimination, despite producing more retrograde damage to the lateral geniculate nuclei than in any monkey with V4 ablation. The visual disorder following removal of visual area V4 strikingly resembles the clinical disorder of mild cerebral achromatopsia with associated apperceptive agnosia for objects and patterns.
We used horseradish peroxidase (HRP) to orthogradely label afferent axons in macaque striate cortex. Of the 38 axons that we recovered, nine were recorded intracellularly before being filled with HRP. Light microscope and computer reconstructions of filled processes reveal highly stereotyped patterns of arborization and suggest that there are at least five discrete populations of lateral geniculate nucleus (LGN) afferent axon: (1) those to layer 4C beta, which have extremely circumscribed, dense terminal fields (small branches of which occasionally intrude into 4C alpha) but which have not been shown to project to other laminae; (2) afferents to layer 4A, which in some cases send fine ascending collaterals into layer 2-3 and which do not, apparently, send collaterals to other laminae; (3) afferents to layer 1, which are fine, extend over large distances horizontally, and send collaterals to layer 6A; (4) afferents to the lower two-thirds of layer 4C alpha, which have few or no collaterals in layer 6; and (5) afferents to the upper half of layer 4C alpha, which have arborizing collaterals in layer 6B. Of the nine axons that were recorded intracellularly, those with projections to layer 4C beta (two axons) and to layer 1 (one axon) had color-selective properties, whereas those (six axons) which arborized in 4C alpha all had transient, broad band and highly contrast-sensitive receptive fields. These properties are consistent with derivations from somata in the parvocellular and magnocellular divisions of the LGN, respectively. Afferents to 4C alpha were found to cover approximately 6 times as much surface area as afferents to 4C beta. The preterminal trunks of all axons were found to follow tortuous paths through the neuropil--paths that may derive from axon segregation during development. The wide ranging, patchy distributions of single afferents in 4C alpha suggest that individual 4C alpha axons supply more than one ocular dominance stripe. In one case where the terminal arborization of a 4C alpha axon was mapped against the transneuronally determined pattern of ocular dominance, three separate patches of terminal boutons were indeed found to coincide with the bands of one eye.
This chapter presents a detailed account of a study conducted on 82 rhesus monkeys with total bilateral ablation of the striate cortex. This study revealed a wide repertoire of visual functions retained or recovered after surgery. The lateral geniculate nuclei of the destriated monkeys contained viable neurons that were identified as local circuit interneurons with ubiquitous membrane properties for developing presynaptic sites at any region of the cell surface. The results of additional lesions demonstrated the critical role assumed by various structures in the absence of striate cortex. The primate striate cortex has a preeminent role in all types of visual functions, with the exception of pupillary and blink reactions. Some sort of reorganization must occur in other structures after striate resections. These studies have influenced significantly the search for residual capacities in humans with lesions of the geniculostriate system, which have revealed a retention or recovery similar to that shown by experimentally damaged monkeys.
In this paper, we shall show that there are substantial numbers of nerve terminals which are normally ineffective. In the intact animal, occasional signs of the postsynaptic effectiveness of these fibres can be seen under conditions of optimal spatial summation or increased excitability or decreased inhibition. If the normally functioning afferent nerve fibres are blocked or cut, some of the previously ineffective fibres immediately establish an effective drive of cells. If the normal afferents are cut and allowed to degenerate, large numbers of cells begin to respond to new inputs. The presence of ineffective synapses in the adult offers an alternative to sprouting or the opening up of polysynaptic pathways as a possible mechanism to explain plasticity of connections in adult brains.
1. We studied the effect of lesions placed in striate cortex or superior colliculus on the detection of visual stimuli and the accuracy of saccadic eye movements. The monkeys (Macaca mulatta) first learned to respond to a 0.25 degrees spot of light flashed for 150-200 ms in one part of the visual field while they were fixating in order to determine if they could detect the light. The monkeys also learned in a different task to make a saccade to the spot of light when the fixation point went out, and the accuracy of the saccades was measured. 2. Following a unilateral partial ablation of the striate cortex in two monkeys they could not detect the spot of light in the resulting scotoma or saccade to it. The deficit was only relative; if we increased the brightness of the stimulus from the usual 11 cd/m2 to 1,700 cd/m2 against a background of 1 cd/m2 the monkeys were able to detect and to make a saccade to the spot of light. 3. Following about 1 mo of practice on the detection and saccade tasks, the monkeys recovered the ability to detect the spots of light and to make saccades to them without gross errors (saccades made beyond an area of +/-3 average standard deviations). Lowering the stimulus intensity reinstated both the detection and saccadic errors...
We examined the retinae of two monkeys whose left striate cortex had been removed eight years previously and compared the transneuronally degenerated hemiretina of each eye with the normal hemiretina, and with the retinae of normal monkeys. All retinae were prepared as whole mounts. One from each pair was stained with Cresyl Violet; the other was reacted for horseradish peroxidase two days after placing pellets of the enzyme in the optic nerve. Measurements of ganglion cell density in the Nissl-stained retina of the contralateral right eye showed that approximately 80% of retinal ganglion cells were missing in the central 30 degrees of the degenerated hemiretinae. More peripherally the percentage loss was less extensive. Measurements of cell soma size and dendritic field size of peroxidase-labelled classified surviving cells in the degenerated temporal hemiretina of the ipsilateral eye showed them to be morphologically normal. In comparison with the normal hemiretina, however, the mean soma size at three selected eccentricities was larger than normal, suggesting selective loss of smaller ganglion cells. Classification of peroxidase-labelled ganglion cells in the normal and degenerated hemiretinae revealed that the population of P beta cells was reduced by as much as 85% in the degenerated region. There was comparable change in the density of P alpha or P gamma cells. The degeneration of the great majority of P beta cells, which are believed to be the morphological substrate of ganglion cells with small and colour-opponent receptive fields, must set limits on the visual sensitivity and discrimination that survive damage to striate cortex.
In the visual field defects of 10 patients who had suffered lesions in the postgeniculate part of the primary visual projection, red-green discrimination and achromatic target detection was tested. In addition, 8 of these patients were tested for detection of red and green targets. Targets were presented on a low photopic achromatic background, so that the red and green targets differed from the background both in intensity and in wavelength, whereas the achromatic target differed in intensity only. Six patients showed evidence of discriminating between red and green targets, 5 patients could also detect the colour targets, but none could detect the achromatic one that was presented at the same retinal position. These results imply that wavelength and intensity information are treated differentially, and suggest that these patients possess residual colour-opponent channels that subserve the defective part of the visual field.
The various structures afferent to area 17 (or V1) of the macaque monkey have widely differing retinotopic organizations. It is likely that these difference are reflected in the topographic organization of the projection from these structures to area V1. We have investigated this issue by placing side‐by‐side injections of two retrograde fluorescent tracers, fast blue and diamidino yellow, in V1. By examining the extent of mixing of the two populations of singly labelled cells and the presence of doubly labelled cells, in different structures, we have characterized the topography of each projection in terms of the size of its axonal arborization and the amount of convergence and divergence.
The afferents from the lateral geniculate nucleus (LGN) and from the pulvinar are organized in a point‐to‐point fashion. The maximum extent of axonal arborization of these afferents is 0.5 mm and these projections demonstrate little scatter (i.e., neighboring LGN neurons project to adjacent regions of V1). The other two subcortical structures examined, the claustrum and the intralaminar nuclei, demonstrate a much larger scatter and wider axonal arborizations in their projections to V1 than do the LGN and pulvinar.
Two‐dimensional reconstructions were made of the distribution of labelled neurons in extrastriate cortical areas. Using the separation between patches of labelled cells and transitions in myelin‐stained sections, we have identified seven separate cortical regions containing labelled cells. Two of these can be identified as area V2 and the middle temporal visual area (MT). Three other regions correspond to areas V3, V3A and V4t. Finally, two more regions of labelling have been distinguished that belong to area V4. These results demonstrate that, at least within the central 6° of visual field, all the presently known extrastriate visual cortical areas project to V1. This result is interesting in view of the fact that only a few extrastriate cortical areas are reported to receive afferents from V1.
Three groups of cortical areas can be distinguished on the basis of the characteristics of their cortical connections to V1. The first group contains area V2, V3, and the posterior region of V4. These areas project to V1 with infra‐ as well as supragranular layer neurons and show limited axonal arborization and scatter in the projection. The second group consists of two regions of labelling in the superior temporal sulcus corresponding to V4t and MT and another on the annectant gyrus (V3A). These regions contain almost exclusively infragranular labelling and show wide axonal‐arborization and scatter in their projections to V1. Finally, the neurons on the prelunate gyrus (V4) appear to have characteristics intermediate between the first two groups.
Examination of the literature reveals that there is a relationship between the receptive field (RF) properties of neurons in different structures afferent to V1 and the geometry of their projection. Structures such as the LGN with small RF size and scatter display point‐to‐point projections to V1. Structures such as the claustrum or area MT that have larger RF size and greater scatter exhibit larger degrees of divergence in their projections to V1.
Horseradish peroxidase was injected intracellularly into single, physiologically‐identified X‐ and Y‐cell geniculocortical axons projecting to area 17 of the cat. This injection anterogradely labeled the axon terminal fields in cortex and retrogradely labeled the somata of these same axons in laminae A and A1 of the lateral geniculate nucleus (LGN). The laminar projections of 21 X‐ and 15 Y‐cell axons were analyzed. For these, the laminar terminations of ten X‐ and seven Y‐cell axons were also related to their cells' positions in the A‐laminae.
The terminal fields of X‐ and Y‐cell axons overlapped substantially in layers IV and VI of area 17. Some X‐cells terminated mainly in IVb, others mainly in IVa, and still others throughout IVa and IVb. The latter two groups also projected up to 100 μm into lower layer III. Y‐cells terminated primarily in layer IVa and projected up to 200 μm into lower layer III. Some also arborized throughout the depth of layer IVb. Both X‐ and Y‐cell axons terminated throughout the depth of layer VI, although more so in the upper half. We found no relationship between the diameter of the parent axon and its sublaminar projection within layer IV.
Within layer IV, X‐cell axons generally terminated within a single, continuous clump and had surface areas of 0.6 to 0.9 mm ² . Axons of Y‐cells often terminated in two to three separate clumps, separated by terminal free gaps 400 to 600 μm wide. Their total surface areas, including gaps, were 1.0 to 1.8 mm ² , roughly 1.6 times the surface areas of X‐cell axons. Despite considerable overlap, Y‐cell arbors contained significantly more boutons than did X‐cell arbors.
The sublaminar projections of the X‐ and Y‐cell axons within layer IV reflected the locations of the cells' somata within the depth of the A‐laminae. X‐cells located in the dorsal or ventral thirds of the depths of the laminae projected mainly to layer IVa or throughout layer IV in cortex. Those located in the central thirds projected mainly to layer IVb. Y‐cells showed a similar positional relationship, but they appeared to follow different rules. Y‐cells in the outer thirds of the A‐laminae projected mainly to layer IVa; those in the central thirds, in addition, expanded their projections to include layer IVb.
In general, larger sized somata in the LGN gave rise to more widely spreading terminal arbors and greater numbers of boutons in cortex than did smaller somata. However, we found no significant relationship between soma size and terminal arbor extent or total boutons within each cell class (X or Y), and thus the correlation noted may result from Y‐cells having larger somata and terminal arbor extents than do X‐cells.
Our results demonstrate considerable heterogeneity in the laminar projections of X‐ and Y‐cell axons within area 17. This heterogeneity reflects an underlying sublaminar organization of the parent somata within the depths of the LGN A‐laminae. The functional significance of this organization, both in the LGN and cortex, is unknown. It is clear, however, that the result of the geniculocortical projection upon layer IV is not to segregate X‐ and Y‐ afferents into lower and upper tiers. Rather, it may be to re‐establish a positional organization existing within the depths of the LGN laminae.
Specific thalamic afferents to visual areas 17 and 18 were physiologically classified as X or Y type and injected with horseradish peroxidase (HRP). The axons were examined under the light microscope and were then processed for correlated electron microscopy. X axons arborized in area 17 and in the border between area 17 and 18. The X axons all formed terminals throughout layer 6, but were heterogeneous in their distribution in layer 4. They either occupied the entire width of sublayers 4A and 4B or were strongly biased toward layer 4A. Y axons also arborized in layers 4 and 6, but in area 17 they did not form boutons in sublamina 4B. Some Y axons projected only to area 18; others branched and arborized in both areas 17 and 18. Only the collaterals of one X axons were found to enter area 18; all the others were restricted to area 17. Y axons formed three to four separate patches of boutons about 300-400 microns in diameter, while all but one X axon formed a single elongated patch. Y axons had thicker main branches (3-4 microns) than X axons (1.5-2.5 microns) at their point of entry to the cortex. The main axon trunks and their medium-calibre collaterals were myelinated, but the preterminal segments were unmyelinated and studded with boutons. Each X or Y axon contacted about seven to ten somata, but Y axons made more contacts per soma (three to six) than did X axons (two to three). In addition to somatic synapses, both X and Y axons formed asymmetric (type 1) synapses on dendritic spines and shafts, with spines forming the most frequent targets (80%). Each Y bouton made, on average, 1.64 synapses in area 17 and 1.79 synapses in area 18, whereas each X bouton made only 1.27 synapses on average. Although there are proportionally fewer Y axons than X axons entering area 17, the Y axons provide as many synapses as the X axons because of their larger arbors and multisynaptic boutons.
The retinal ganglion cells were counted in a rhesus monkey from which the striate cortex had been removed 8 years earlier, and the results compared with those obtained previously with the eyes of normal monkeys. About 80% of the ganglion cells within 10 degrees of the fovea were missing. Peripherally their density was unaffected. The ganglion cell layer of the entire retina resembled the peripheral retina of a normal monkey, and this result helps to explain the remarkable nature of the animal's vision.
By injecting the enzyme horseradish peroxidase into the prestriate
cortex of the macaque monkey and examining the lateral geniculate
nucleus (l.g.n.) for retrograde label, the presence of a direct
projection from the l.g.n. to prestriate visual cortex (Brodmann's areas
18 and 19) was confirmed. Labelled cells occurred in all layers of the
l.g.n., distributed in a roughly columnar fashion. The large scatter in
cell distribution indicated a lower retinotopic precision for this
projection than for the one to area 17. Labelled cells are of a medium
to large size and, in each section, a few were located near the laminar
border or in interlaminar zones. The functional significance of this
projection is discussed.
Recent publications have demonstrated a projection of the lateral geniculate nucleus (LGN) onto extrastriate cortical regions in the old world monkey but have failed to identify a projection from this nucleus to V2, the area adjacent to the striate cortex. In this report we show that such a projection exists, as demonstrated by the retrograde transport of the fluorescent labels fast blue (FB) and diamidino yellow (DY). Neurons labelled after V2 injections are more scattered in the LGN than the cells backfilled by the V1 injections and mostly belong to the interlaminar zones and the S layers, regions which are largely devoid of neurons labelled by the V1 injections.
Both anterograde (autoradiographic) and retrograde (horseradish peroxidase) tracing techniques were used to identify and characterize projections from the dorsal lateral geniculate nucleus (DLG) of the thalamus to the subdivisions of occipital prestriate cortex (generally defined by areas 18 and 19) in macaque monkeys. It was found that the DLG projects to area 19 and the anterior portion of area 18 located on the lateral, ventral, and ventromedial surfaces of the hemisphere. There is a general topographical organization such that the medial portion of the DLG projects to dorsal prestriate located between the lunate and superior temporal sulci, while the lateral portion of the DLG projects to ventral prestriate extending from the inferior occipital to the occipitotemporal sulci. The DLG projects to most of the occipitotemporal sulcus. In contrast DLG inputs to the lunate, superior temporal, and inferior occipital sulci are limited in extent, and involve only a portion of the bank or shoulder of each sulcus which is continuous with the cortex located on the surfaces of the surrounding preoccipital gyri. The projection to the inferior occipital sulcus is more extensive than the ones to the lunate and superior temporal sulci and involves the floor as well as the ventral bank. This means that there are certain functional subdivisions, such as those located within the lunate (eg, visual area 2) and superior temporal sulci which do not receive DLG input. Regardless of the location of these projections the terminal pattern was the same and occurred in horizontally segregated "patches" which were restricted to layer V and the lower, adjacent portion of layer IV. In contrast, the projections from the nearby pulvinar to cortical layers IV, III, and I of the same prestriate areas do not overlap with those from the DLG. An attempt was made to identify possible afferent inputs to these DLG-prestriate paths. The HRP experiments reveal that the DLG-prestriate cells are concentrated in the DLG interlaminar zones and that their distribution overlaps the distribution of terminals from the superior colliculus and, as shown previously, prestriate cortex. Intraocular injections of radioactive precursors demonstrated transsynaptic transport to a number of structures except prestriate cortex. While the latter result does not prove that the DLG-prestriate cells do not receive retinal input, one conclusion is that the DLG-prestriate projection could be organized like pulvino-prestriate systems which receive their inputs from the midbrain and cortex.
Horseradish peroxidase was deposited in the optic nerve to retrogradely label and reveal the dendritic form of all classes of ganglion cell, or it was injected into the dorsal lateral geniculate nucleus to reveal only those classes projecting to the thalamus. The results were compared with those of the accompanying paper in which the ganglion cells projecting to the midbrain are selectively revealed. Two major classes of ganglion cells are described, the Pα and Pβ cells. For both classes dendritic field size increases with eccentricity from the fovea and there is no overlap in the two classes at any given eccentricity. Cell body size shows a similar mean difference but with a slight overlap. Both cell bodies and dendritic fields are larger along the temporal horizontal meridian than the nasal horizontal meridian, for Pα and for Pβ cells, but these differences are reduced when naso-temporal differences in ganglion cell density are taken into account, that is, size correlates closely with density. Injections restricted to the parvocellular layers of the lateral geniculate nucleus labelled almost exclusively Pβ cells, whereas injections confined to the magnocellular layers labelled almost exclusively Pα cells. As midbrain injections label no Pβ cells and few Pα cells it can be shown that about 80% of ganglion cells are Pβ cells projecting to parvocellular lateral geniculate nucleus, and that about 10% are Pα cells projecting to magnocellular layers. The coverage factor, that is the number of cells covering each point on the retina, varied from 1.9–2.3 for Pβ cells, and from 2–7 for Pα cells.
Two‐dimensional maps of individual layers of the dorsal lateral geniculate nucleus (LGN) in the macaque monkey were constructed and used as a basis for comparing laminar size, shape, and topographic organization. Topographical data from the electrophysiological investigation of the LGN by Malpeli and Baker ('75) were displayed on maps of all six layers. As known from previous studies, there is a significant over‐representation of central vision in the LGN. Unexpectedly, though, the visual representation is anisotropic over portions of most LGN layers. That is, the linear magnification factor (millimeters along the laminar surface per degree of visual field) is not equal for all directions from a given point in the visual field. Moreover, the visual representations in the parvicellular and magnocellular divisions of the LGN differ both in their emphasis on central vision and in their anisotropies.
To determine the degree of individual variability, laminar maps were prepared from the LGN of seven other hemispheres. The shapes of laminar maps varied considerably between LGNs, from nearly circular to highly elliptical, but the surface area was relatively constant for each layer. Topographical organization, determined by mapping the optic disc representation on the LGN laminae and by labeling from anterograde and retrograde tracer injections in striate cortex, showed significant individual variability.
Interestingly, the visual representations in the LGN and striate cortex are topologically inverted with respect to one another. This indicates that the establishment of geniculocortical connections involves a systematic crossing‐over of fibers.
Information on cell densities and magnification factors in striate cortex obtained from other studies was compared to the results of the present study in order to estimate ratios of cortical neurons to LGN neurons at different eccentricities. The total number of cortical neurons per LGN neuron is about 130 on average, but it extends over approximately a tenfold range, from less than 100 in the far periphery to nearly 1,000 in the fovea. The estimated number of cells in layers 4A and 4Cβ per parvicellular layer neuron is smaller and extends over a slightly narrower range, from 30 to 240, whereas the number of layer 4Cα neurons per magnocellular neuron varies more widely, from about 45 to 7,000.
The enzyme horseradish peroxidase (HRP) was separately injected into striate, prestriate, inferotemporal, and parietal cortices in 19 macaque monkeys, and the lateral geniculate nucleus (LGN) was examined for retrograde transport. Labeled LGN cells were identified only in the animals, with HRP injections into the striate and prestriate cortex. Following injections into either of these regions, labeled cells were found in both parvocellular and magnocellular regions of the ipsilateral LGN only, in keeping with the topographic relation of HRP injection sites in the cortex to labeled areas in the LGN. It was also found that (1) labeled LGN cells were less numerous in both laminar and interlaminar zones following HRP injection into the prestriate cortex, whereas following HRP injection into the striate cortex labeled cells were found almost exclusively in the laminae, and localized to a wedge-shaped region; (2) following HRP injection into the prestriate cortex, the mean sizes of the labeled parvocellular and magnocellular cells, estimated in projected diameter, were almost the same, these means being significantly larger than the mean size of labeled parvocellular cells and much smaller than that of labeled magnocellular cells following HRP injection into the striate cortex; (3) the shapes of the labeled LGN cells following HRP injection into the prestriate cortex were ovoid, fusiform, or triangular (or multipolar), whereas those following HRP injection into the striate cortex were uniformly ovoid or round. The above findings following HRP injections into the prestriate cortex in normal monkeys were confirmed by HRP injections into the prestriate cortex of monkeys whose striate cortex had been removed several months prior to the injection; labeled cells were found in confines of areas of retrograde degeneration in the LGN and their labeling pattern was the same as that in intact animals. It was concluded that in macaque monkeys, just as in the cat, a geniculoprestriate projection system exists; it was suggested that there are two parallel system of visual information processing from the LGN to the prestriate cortex, a direct one and in indirect one through the striate cortex.
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