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Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus
Abstract
Superior colliculus lesions had little effect on the visual response of neurons in the monkey inferior pulvinar. By contrast, striate cortex lesions eliminated the visual response of all inferior pulvinar neurons for a period of 3 weeks after the lesion. At longer survival times, a few pulvinar neurons responded to small light spots, but sensitivity to orientation and direction of movement never returned. Thus striate cortex, rather than the colliculus, appears to be responsible for the visual properties of pulvinar cells.
... 7 Experiments demonstrating V1 driving influences on the pulvinar, as well as of the cortex on other HO thalamic nuclei, have relied on inferences following complete (chronic or transient) cortical inactivation. [21][22][23][24][25][26] However, these non-specific approaches would be expected to affect both L5 and L6 CT pathways, as well as activity in other cortical areas and subcortical structures. Thus, the functional consequences of these different classes of inputs to the HO thalamus are not known and might differ considerably from the FO thalamus. ...
... Meanwhile, our primary strategy for silencing L5 CT projections was to use the Npr3-Cre mouse line to restrict inhibitory opsin expression to L5ET neurons in V1. This offers a marked improvement in specificity from other studies that have relied on non-specific cortical inactivation, [22][23][24][25] which would be expected to also suppress activity in other cortical areas 69 and thus confound the driving influence of V1, specifically L5ETs, on the pulvinar with that of the extrastriate cortex. Indeed, we observed somewhat more widespread pulvinar inactivation when we non-specifically inactivated the cortex, even when that inactivation was confined to V1 through AAV injection (Figures S6A-S6F). ...
... This idea is in line with evidence that the rodent pulvinar conveys contextual information (e.g., a mismatch between visual flow and running speed) to extrastriate areas 5 and even back to V1. 4 It is notable, however, that SC inactivation/lesion was shown to considerably impair visual responses in regions of the pulvinar homologous to the mouse lPulv 52 in rabbits 59 but not in macaque monkeys. 25 It is therefore possible that subcortical inputs might play a more prominent role in shaping pulvinar visual response properties in non-primates. 59 Altogether, our results demonstrate a striking functional dissociation between L6 and L5 CT pathways. ...
Higher-order (HO) thalamic nuclei interact extensively and reciprocally with the cerebral cortex. These corticothalamic (CT) interactions are thought to be important for sensation and perception, attention, and many other important brain functions. CT projections to HO thalamic nuclei, such as the visual pulvinar, originate from two different excitatory populations in cortical layers 5 and 6, whereas first-order nuclei (such as the dorsolateral geniculate nucleus; dLGN) only receive layer 6 CT input. It has been proposed that these layer 5 and layer 6 CT pathways have different functional influences on the HO thalamus, but this has never been directly tested. By optogenetically inactivating different CT populations in the primary visual cortex (V1) and recording single-unit activity from V1, dLGN, and pulvinar of awake mice, we demonstrate that layer 5, but not layer 6, CT projections drive visual responses in the pulvinar, even while both pathways provide retinotopic, baseline excitation to their thalamic targets. Inactivating the superior colliculus also suppressed visual responses in the same subregion of the pulvinar, demonstrating that cortical layer 5 and subcortical inputs both contribute to HO visual thalamic activity—even at the level of putative single neurons. Altogether, these results indicate a functional division of “driver” and “modulator” CT pathways from V1 to the visual thalamus in vivo.
... L5CTs are thus frequently referred to as "drivers" and L6CTs as "modulators" of HO nuclei (Sherman, 2016;Sherman and Guillery, 2002), but whether these parallel CT projection pathways are functionally distinct has never been directly tested (Bickford, 2015). Experiments demonstrating V1 driving influences on the pulvinar, as well as of the cortex on other HO thalamic nuclei, have relied on inferences following complete (chronic or transient) cortical inactivation (Beltramo and Scanziani, 2019;Bender, 1983;Bennett et al., 2019;Casanova et al., 1997;Diamond et al., 1992;Mease et al., 2016). However, these non-specific approaches would be expected to affect both L5 and L6 CT pathways, as well as activity in other cortical areas and subcortical structures. ...
... Meanwhile, our primary strategy for silencing L5 CT projections was to use the Npr3-Cre mouse line to restrict inhibitory opsin expression to L5ET neurons in V1. This offers a marked improvement in specificity from other studies that have relied on non-specific cortical inactivation (Beltramo and Scanziani, 2019;Bender, 1983;Bennett et al., 2019;Casanova et al., 1997), which would be expected to also suppress activity in other cortical areas (Leopold, 2012) and thus confound the driving influence of V1, specifically L5ETs, on the pulvinar with that of extrastriate cortex. Indeed, we observed somewhat more widespread pulvinar inactivation when we non-specifically inactivated cortex, even when that inactivation was confined to V1 through AAV injection (FigureS S5A-F). ...
... This idea is in line with evidence that the rodent pulvinar conveys contextual information (e.g., a mismatch between visual flow and running speed) to extrastriate areas and even back to V1 (Roth et al., 2016). It is notable, however, that SC inactivation/lesion was shown to considerably impair visual responses in regions of the pulvinar homologous to the mouse lPulv (Baldwin et al., 2017) in rabbits (Casanova and Molotchnikoff, 1990), but not in macaques (Bender, 1983). It is therefore possible that subcortical inputs might play a more prominent role in shaping pulvinar visual response properties in non-primates (Casanova and Molotchnikoff, 1990). ...
Higher-order (HO) thalamic nuclei interact extensively with the cerebral cortex and are innervated by excitatory corticothalamic (CT) populations in layers 5 and 6. While these distinct CT projections have long been thought to have different functional influences on the HO thalamus, this has never been directly tested. By optogenetically inactivating different CT populations in the primary visual cortex (V1) of awake mice, we demonstrate that layer 5, but not layer 6, CT projections drive visual responses in the HO visual pulvinar, even while both pathways provide retinotopic, baseline excitation to their thalamic targets. Inactivating the superior colliculus also suppressed visual responses in the pulvinar, demonstrating that cortical layer 5 and subcortical inputs both contribute to HO visual thalamic activity - even at the level of putative single neurons. Altogether, these results indicate a functional division of driver and modulator CT pathways from V1 to the visual thalamus in vivo.
... This holds true for the LGN, which targets layer 4 in V1 and receives feedback modulatory signals from layer 6 [50]. While it is generally accepted that pulvinar neurons in primates and cats receive driver inputs from V1 [51,52], and in turn send modulatory signals to layer 1 [53,54], it is still unknown if corticothalamic pathways involving higher-order areas and the pulvinar conform with the driver/modulator framework, despite recent findings of hierarchical anatomical organization of cortico-pulvinar projections in cats [18]. Addressing this issue is especially challenging since pulvinar axon terminals or cortical cell bodies are generally not restricted to a single cortical layer [55,56]. ...
... In cats and monkeys, findings from neuronal inactivation studies align with corticothalamic anatomical features. Silencing V1, for instance, abolishes visual responses in most pulvinar neurons in cats and monkeys [51,52], underscoring the notion of V1 as a driver of pulvinar activity. Conversely, considering our previous anatomical discussion, higher-order cortical areas are believed to primarily modulate pulvinar activity. ...
The pulvinar nucleus of the thalamus is a crucial component of the visual system and plays significant roles in sensory processing and cognitive integration. The pulvinar’s extensive connectivity with cortical regions allows for bidirectional communication, contributing to the integration of sensory information across the visual hierarchy. Recent findings underscore the pulvinar’s involvement in attentional modulation, feature binding, and predictive coding. In this review, we highlight recent advances in clarifying the pulvinar’s circuitry and function. We discuss the contributions of the pulvinar to signal modulation across the global cortical network and place these findings within theoretical frameworks of cortical processing, particularly the global neuronal workspace (GNW) theory and predictive coding.
... Where does this information go after being Frontiers in Neural Circuits | www.frontiersin.org Hoogland et al., 1991;Veinante et al., 2000;Groh et al., 2008Groh et al., , 2013Theyel et al., 2010;Guo et al., 2017Guo et al., , 2020Sumser et al., 2017;Mo and Sherman, 2019;Prasad et al., 2020;Sampathkumar et al., 2021 Bourassa andDeschenes, 1995;Li et al., 2003c;Masterson et al., 2009;Stitt et al., 2018;Bennett et al., 2019;Prasad et al., 2020;Blot et al., 2021Ojima, 1994Bartlett et al., 2000;Rouiller and Welker, 2000;Sherman, 2008, 2009;Williamson and Polley, 2019;Pardi et al., 2020Xiao et al., 2009Collins et al., 2018;Prasad et al., 2020;Anastasiades et al., 2021 L5-HO synaptic/intrinsic physiology Reichova and Sherman, 2004;Landisman and Connors, 2007;Groh et al., 2008;Theyel et al., 2010;Seol and Kuner, 2015;Mease et al., 2017;Guo et al., 2020;Desai andVarela, 2021 Li et al., 2003a,b;de Souza et al., 2019;Desai and Varela, 2021Desai and Varela, 2021Collins et al., 2018Anastasiades et al., 2021TC anatomy Koralek et al., 1988Lu and Lin, 1993;Bureau et al., 2006;Groh et al., 2010;Meyer et al., 2010a;Theyel et al., 2010;Wimmer et al., 2010;Viaene et al., 2011;Audette et al., 2017;Casas-Torremocha et al., 2019;Sermet et al., 2019;El-Boustani et al., 2020;Rodriguez-Moreno et al., 2020Saalmann et al., 2012Stitt et al., 2018;Bennett et al., 2019Pardi et al., 2020Delevich et al., 2015Collins et al., 2018;Mukherjee et al., 2020;Anastasiades et al., 2021 TC physiology Bureau et al., 2006;Lee and Sherman, 2008;Petreanu et al., 2009;Theyel et al., 2010;Audette et al., 2017;Casas-Torremocha et al., 2019;Mo and Sherman, 2019;Sermet et al., 2019;El-Boustani et al., 2020;Guo et al., 2020Purushothaman et al., 2012Stitt et al., 2018 Lee andPardi et al., 2020Delevich et al., 2015Collins et al., 2018;Anastasiades et al., 2021 L5 CTC function in vivo Groh et al., 2013;Gambino et al., 2014;Mease et al., 2016a,b,c;Rojas-Piloni et al., 2017;Audette et al., 2019;Williams and Holtmaat, 2019;Zhang and Bruno, 2019;LaTerra et al., 2020;Suzuki and Larkum, 2020;Takahashi et al., 2020;Pagès et al., 2021Bender, 1983Purushothaman et al., 2012;Saalmann et al., 2012;Stitt et al., 2018;Yu et al., 2018;Bennett et al., 2019;de Souza et al., 2019;Blot et al., 2021;Kirchgessner et al., 2021Asokan et al., 2018Williamson and Polley, 2019;Pardi et al., 2020Parnaudeau et al., 2013Schmitt et al., 2017;Rikhye et al., 2018;Mukherjee et al., 2020 Recent studies using cell-type-specific approaches are emphasized. ...
... As Table 1 reflects, the somatosensory HO CTC circuit has provided a wealth of recent anatomical and functional data on cell-type-specific interactions and the in vivo impact of HO thalamus on cortical function. In the visual system, the pulvinar nucleus (PuV) [or the homologous LP nucleus in rodents] is the L5tt-receiving HO nucleus, and is connected to all visual cortices (Bender, 1983;Saalmann et al., 2012;Bennett et al., 2019;de Souza et al., 2019). While pulvinar has been largely studied in primates, recent cell-type-specific and optogenetic studies have made increasing use of mouse models ( Table 1). ...
Large portions of the thalamus receive strong driving input from cortical layer 5 (L5) neurons but the role of this important pathway in cortical and thalamic computations is not well understood. L5-recipient “higher-order” thalamic regions participate in cortico-thalamo-cortical (CTC) circuits that are increasingly recognized to be (1) anatomically and functionally distinct from better-studied “first-order” CTC networks, and (2) integral to cortical activity related to learning and perception. Additionally, studies are beginning to elucidate the clinical relevance of these networks, as dysfunction across these pathways have been implicated in several pathological states. In this review, we highlight recent advances in understanding L5 CTC networks across sensory modalities and brain regions, particularly studies leveraging cell-type-specific tools that allow precise experimental access to L5 CTC circuits. We aim to provide a focused and accessible summary of the anatomical, physiological, and computational properties of L5-originating CTC networks, and outline their underappreciated contribution in pathology. We particularly seek to connect single-neuron and synaptic properties to network (dys)function and emerging theories of cortical computation, and highlight information processing in L5 CTC networks as a promising focus for computational studies.
... Most of the rest of the visual pulvinar consists of two large retinotopically organized nuclei that mirror each other, PIcl and PL (galagos: [31,54]; owl monkeys: [22]; cebus monkeys: [24]; macaque monkeys: [23,25]; humans: [45,55]. Both nuclei depend on direct and indirect inputs from V1, but not the superior colliculus, for activation [56]. In agreement, the receptive fields of neurons in these nuclei reflect those of neurons in V1 and not those of neurons in the superior colliculus [56,57]. ...
... Both nuclei depend on direct and indirect inputs from V1, but not the superior colliculus, for activation [56]. In agreement, the receptive fields of neurons in these nuclei reflect those of neurons in V1 and not those of neurons in the superior colliculus [56,57]. While in primates, the superior colliculus does project to both PIcl and PL, the projections are relatively sparse and species variable [52] and they express little or no VGLUT2 in their terminals [33][34][35]51]. ...
Current evidence supports the view that the visual pulvinar of primates consists of at least five nuclei, with two large nuclei, lateral pulvinar ventrolateral (PLvl) and central lateral nucleus of the inferior pulvinar (PIcl), contributing mainly to the ventral stream of cortical processing for perception, and three smaller nuclei, posterior nucleus of the inferior pulvinar (PIp), medial nucleus of the inferior pulvinar (PIm), and central medial nucleus of the inferior pulvinar (PIcm), projecting to dorsal stream visual areas for visually directed actions. In primates, both cortical streams are highly dependent on visual information distributed from primary visual cortex (V1). This area is so vital to vision that patients with V1 lesions are considered “cortically blind”. When the V1 inputs to dorsal stream area middle temporal visual area (MT) are absent, other dorsal stream areas receive visual information relayed from the superior colliculus via PIp and PIcm, thereby preserving some dorsal stream functions, a phenomenon called “blind sight”. Non-primate mammals do not have a dorsal stream area MT with V1 inputs, but superior colliculus inputs to temporal cortex can be more significant and more visual functions are preserved when V1 input is disrupted. The current review will discuss how the different visual streams, especially the dorsal stream, have changed during primate evolution and we propose which features are retained from the common ancestor of primates and their close relatives.
... We know that V1 provides a strong driver input to the pulvinar from layer 5 complex cells (Casanova, 1993). Permanent or transient inactivation of V1 results in an almost total disappearance of visual responses in the striate-recipient zone of the pulvinar in cats and primates, indicating that V1 is necessary for establishing the fundamental representation of the visual world in the pulvinar (Bender, 1983;Casanova et al., 1997). The contribution of other areas to the subregions of the pulvinar is still not fully understood. ...
In most neuroscience textbooks, the thalamus is presented as a structure that relays sensory signals from visual, auditory, somatosensory, and gustatory receptors to the cerebral cortex. But the function of the thalamic nuclei goes beyond the simple transfer of information. This is especially true for the second-order nuclei, but also applies to first-order nuclei. First order thalamic nuclei receive information from the periphery, like the dorsal lateral geniculate nucleus (dLGN), which receives a direct input from the retina. In contrast, second order thalamic nuclei, like the pulvinar, receive minor or no input from the periphery, with the bulk of their input derived from cortical areas. The dLGN refines the information received from the retina by temporal decorrelation, thereby transmitting the most “relevant” signals to the visual cortex. The pulvinar is closely linked to virtually all visual cortical areas, and there is growing evidence that it is necessary for normal cortical processing and for aspects of visual cognition. In this article, we will discuss what we know and do not know about these structures and propose some thoughts based on the knowledge gained during the course of our careers. We hope that these thoughts will arouse curiosity about the visual thalamus and its important role, especially for the next generation of neuroscientists.
... The activation in V2 could be caused by a cortico-cortical single synaptic connection (e.g. V1-V2) or it can be caused by polysynaptic signal propagation (cortico-thalamocortical connections; (Bender 1983;Hilgetag et al. 2000a;Hilgetag et al. 2000b;Rushmore et al. 2005)). Moreover, due to the temporal resolution we used, we cannot distinguish between the orthodromic and antidromic activation of V2, however, the similarity between the visually evoked maps and ICMS-evoked maps (Supplementary Fig. S1) suggest a major orthodromic activation from V1 to V2. ...
Intracortical microstimulation (ICMS) in the primary visual cortex (V1) can generate the visual perception of a small point of light, termed phosphene, and evoke saccades directed to the receptive field of the stimulated neurons. Although ICMS is widely used, a direct measurement of the spatio-temporal patterns of neural activity evoked by ICMS and their relation to the neural responses evoked by visual stimuli or how they relate to ICMS-evoked saccades are still missing. To investigate this, we combined ICMS with voltage-sensitive dye imaging in V1 of behaving monkeys and measured neural activity at a high spatial (meso-scale) and temporal resolution. We then compared the population response evoked by small visual stimuli to those evoked by microstimulation. Both stimulation types evoked population activity that spread over few millimeters in V1 and propagated to extrastriate areas. However, the population responses evoked by ICMS have shown faster dynamics for the activation transients and the horizontal propagation of activity revealed a wave-like propagation. Finally, neural activity in the ICMS condition was higher for trials with evoked saccades as compared with trials without saccades. Our results uncover the spatio-temporal patterns evoked by ICMS and their relation to visual processing and saccade generation.
... In the visual system of large mammals, the pulvinar is the most prominent HO nuclei and it establishes reciprocal connections with virtually all visual cortical areas of the neocortex (Shipp, 2003;Sherman and Guillery, 2011). This connectivity is reflected in the response properties of pulvinar neurons, which resembles those found in visual cortical cells at different hierarchical levels (Bender, 1983;Casanova, 2003Casanova, , 2021Le et al., 2019). It has been recently suggested that the unique network created between the pulvinar and the cortex is used to mediate the temporality of cortical communication (Saalmann et al., 2012;Fiebelkorn et al., 2019;Cortes et al., 2020). ...
Two types of corticothalamic (CT) terminals reach the pulvinar nucleus of the thalamus, and their distribution varies according to the hierarchical level of the cortical area they originate from. While type 2 terminals are more abundant at lower hierarchical levels, terminals from higher cortical areas mostly exhibit type 1 axons. Such terminals also evoke different excitatory postsynaptic potential dynamic profiles, presenting facilitation for type 1 and depression for type 2. As the pulvinar is involved in the oscillatory regulation between intercortical areas, fundamental questions about the role of these different terminal types in the neuronal communication throughout the cortical hierarchy are yielded. Our theoretical results support that the co-action of the two types of terminals produces different oscillatory rhythms in pulvinar neurons. More precisely, terminal types 1 and 2 produce alpha-band oscillations at a specific range of connectivity weights. Such oscillatory activity is generated by an unstable transition of the balanced state network’s properties that it is found between the quiescent state and the stable asynchronous spike response state. While CT projections from areas 17 and 21a are arranged in the model as the empirical proportion of terminal types 1 and 2, the actions of these two cortical connections are antagonistic. As area 17 generates low-band oscillatory activity, cortical area 21a shifts pulvinar responses to stable asynchronous spiking activity and vice versa when area 17 produces an asynchronous state. To further investigate such oscillatory effects through corticothalamo-cortical projections, the transthalamic pathway, we created a cortical feedforward network of two cortical areas, 17 and 21a, with CT connections to a pulvinar-like network with two cortico-recipient compartments. With this model, the transthalamic pathway propagates alpha waves from the pulvinar to area 21a. This oscillatory transfer ceases when reciprocal connections from area 21a reach the pulvinar, closing the CT loop. Taken together, results of our model suggest that the pulvinar shows a bi-stable spiking activity, oscillatory or regular asynchronous spiking, whose responses are gated by the different activation of cortico-pulvinar projections from lower to higher-order areas such as areas 17 and 21a.
... In terms of the brain regions responsible for blindsight, the observation with extensive ablation of the cortical tissue suggests the totally subcortical processing for some visuomotor functions (Tomaiuolo et al., 1997;Savina and Guitton, 2018); but other studies suggest the involvement of cortical visual processing for goal-directed movements in the blindsight subjects (monkeys: Schmid et al., 2010;Bridge et al., 2019;humans: Ajina et al., 2015;Ajina and Bridge, 2018). As for the visual pathway to the cortex, the earlier studies focused on the role of the superior colliculus (SC)-pulvinar-extrastriate pathway to bypass the V1 (Diamond and Hall, 1969;Bender, 1983Bender, , 1988Warner et al., 2015). The role of SC has been repeatedly confirmed both in monkeys (Mohler and Wurtz, 1977;Rodman et al., 1990;Kato et al., 2011) and in human patients (Leh et al., 2010;Georgy et al., 2016). ...
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.
... Indeed, the disynaptic route from the superior colliculus to amygdala through LP that exists in mice (Wei et al., 2015) has not been observed in the primate pulvinar (Linke et al., 1999;Pessoa and Adolphs, 2010). Moreover, unlike pLP which inherits many of its functional properties from SC and where SC inactivations have a strong effect, activity in inferior pulvinar is primarily inherited from its cortical inputs (Berman and Wurtz, 2011), and SC silencing does not have a strong effect (Bender, 1983). Nevertheless, the rough mapping outlined above is interesting to keep in mind when reviewing the functional correlates of LP and pulvinar. ...
The lateral posterior nucleus of the thalamus (LP) occupies an enigmatic position in the visual processing hierarchy. It both receives its driving input from primary visual cortex (V1) and sends extensive diffuse feedback projections back to the same area. While LP and its primate homolog, the pulvinar, have been implicated in a host of visual and motor behaviors, its function in rodents and the signals it sends to V1 remain mostly uncharacterized. In order to investigate this nucleus and the information it sends to V1, we recorded LP projections to V1 during two different visual paradigms in mice (Mus musculus). We then compared the signals sent by LP to V1 with the information found in V1 neurons, both in layer (L)2/3 and L5.
The first paradigm investigated how LP and V1 visual responses incorporate proprioceptive information about the position of the body relative to the head. Integration of head-on-body position is vital for localizing visual stimuli relative to the body, but has not previously been shown in primary visual circuits in rodents. We developed a paradigm for measuring modulation of visual responses by neck proprioception following changes in head-body angle. Visual responses of LP→V1 projections, V1 L2/3 neurons and V1 L5 neurons that project back to LP showed modulation by body position. These modulations resembled body position gain fields, a canonical neural computation that has been extensively described in sensorimotor transformations in primates.
In the second project, we recorded signals sent by LP to V1 in a visual motion discrimination task. Mice learned to report the dominant direction of motion of a random dot stimulus by licking one of two lickspouts. LP→V1 projections responded during all parts of the task, including heightened activity before the stimulus, as well as stimulus- and choice-specific responses. Individual pre-synaptic boutons often showed a combination of tunings across task-relevant parameters, similarly to neurons in cortical association areas. V1 neurons by contrast predominantly encoded the stimulus. Visual properties of LP→V1 projections reflected the sensory properties of V1 L5 neurons. LP projections to V1 therefore incorporated sensory signals from their primary driving input with choice signals to provide diverse information to V1.
One of the main techniques used throughout this research was axonal imaging of calcium transients following neuronal activity. However axonal imaging is difficult because calcium indicator molecules diffuse poorly to distal axons, which leads to dim images with a low signal-to-noise (SNR), particularly in thalamocortical axons. Therefore a part of this research was dedicated to characterizing an improved calcium indicator for axonal imaging. The result was the axon-GCaMP6 family, a genetically encoded calcium sensor which is actively transported to the axon. This sensor has
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a brighter baseline in axonal compartments and yields a higher SNR and improved motion correction capabilities in thalamocortical axons.
Our findings suggest that LP sends diverse information in its projections to V1, including visual and motor signals which are specific for lateralized motor behaviors. LP also shows modulation of its visual responses by proprioceptive information that is crucial for visually guided actions. These likely serve as important contextual signals for the downstream neurons in V1.
... Monkeys retain saccadic eye movements toward a target in their blind field after a V1 lesion, but this ability and the potential for recovery is lost if the ipsilesional superior colliculus is also inactivated (30,31). Similarly, superior colliculus neurons may retain their response to visual stimulation after striate cortex removal, although this response becomes considerably weaker (31)(32)(33)(34). In human studies, a critical role has been suggested in motion blindsight after brain damage at birth or in early childhood (35)(36)(37), while the LGN appears critical for adult-onset cortical blindness (13,15). ...
Humans can respond rapidly to viewed expressions of fear, even in the absence of conscious awareness. This is demonstrated using visual masking paradigms in healthy individuals and in patients with cortical blindness due to damage to the primary visual cortex (V1) - so called affective blindsight. Humans have also been shown to implicitly process facial expressions representing important social dimensions. Two major axes, dominance and trustworthiness, are proposed to characterize the social dimensions of face evaluation. The processing of both types of implicit stimuli is believed to occur via similar subcortical pathways involving the amygdala. However, we do not know whether unconscious processing of more subtle expressions of facial traits can occur in blindsight, and if so, how. To test this, we studied 13 patients with unilateral V1 damage and visual field loss. We assessed their ability to detect and discriminate faces that had been manipulated along two orthogonal axes of trustworthiness and dominance to generate five trait levels inside the blind visual field: dominant, submissive, trustworthy, untrustworthy, and neutral. We compared neural activity and functional connectivity in patients classified as blindsight positive or negative for these stimuli. We found that dominant faces were most likely to be detected above chance, with individuals demonstrating unique interactions between performance and face trait. Only patients with blindsight (n = 8) showed significant preference in the superior colliculus and amygdala for face traits in the blind visual field, and a critical functional connection between the amygdala and superior colliculus in the damaged hemisphere. We also found a significant correlation between behavioral performance and fMRI activity in the amygdala and lateral geniculate nucleus across all participants. Our findings confirm that affective blindsight involving the superior colliculus and amygdala extends to the processing of socially salient but emotionally neutral facial expressions when V1 is damaged. This pathway is distinct from that which supports motion blindsight, as both types of blindsight can exist in the absence of the other with corresponding patterns of residual connectivity.
... (C) A general schematic of the changing proportion of type I and type II CT projections as a function of cortical hierarchy. et al.1997;Rushmore et al. 2005;Bennett et al. 2019;Bender 1983), suggesting a common ground of functional organization among species. ...
Signals from lower cortical visual areas travel to higher order areas for further processing through corticocortical projections, organized in a hierarchical manner. These signals can also be transferred between cortical areas via alternative cortical transthalamic routes involving higher order thalamic nuclei like the pulvinar. It is unknown whether the organization of transthalamic pathways may reflect the cortical hierarchy. Two axon terminals types have been identified in cortico-thalamic (CT) pathways: the types I (modulators) and II (drivers) characterized by thin axons with small terminals and by thick axons and large terminals, respectively. In cats, projections from V1 to the pulvinar comprise mainly type II terminals whereas those from extrastriate areas include a combination of both terminals suggesting that the nature of CT terminals varies with the hierarchical order of visual areas. To test this hypothesis, distribution of CT terminals from area 21a was charted and compared with three other visual areas located at different hierarchical levels. Results demonstrate that the proportion of modulatory CT inputs increases along the hierarchical level of cortical areas. This organization of transthalamic pathways reflecting cortical hierarchy provides new and fundamental insights for the establishment of more accurate models of cortical signal processing along transthalamic cortical pathways.
... As the temporal resolution we used our experiments is 10 ms, the latency of the measured response in extrastriate cortex cannot determine the exact propagation circuitry. The activation in V2 can be caused by corticocortical single synaptic connection or it can be caused by polysynaptic signal propagation (cortico-thalamo-cortical connections (Bender, 1983;C. Hilgetag, Burns, O'Neill, Scannell, & Young, 2000;C. ...
Intra cortical microstimulation (ICMS) in the primary visual cortex (V1) can generate the visual perception of phosphenes and evoke saccades directed to the stimulated location in the retinotopic map. Although ICMS is widely used, little is known about the evoked spatio-temporal patterns of neural activity and their relation to neural responses evoked by visual stimuli or saccade generation. To investigate this, we combined ICMS with Voltage Sensitive Dye Imaging in V1 of behaving monkeys and measured neural activity at high spatial (meso-scale) and temporal resolution. Small visual stimuli and ICMS evoked population activity spreading over few mm that propagated to extrastriate areas. The population responses evoked by ICMS showed faster dynamics and different spatial propagation patterns. Neural activity was higher in trials w/saccades compared with trials w/o saccades. In conclusion, our results uncover the spatio-temporal patterns evoked by ICMS and their relation to visual processing and saccade generation.
... The functional contribution of projections from SC is more studied in the ventral pulvinar. Specifically, extensive lesions of SC caused only little effect on visual responses in the ventral pulvinar, compared with striate cortex lesions (Bender 1983). In rabbits, however, the inactivation of SC led to a strong attenuation of responses in lateral posterior (LP) nucleus (which is a part of the LP-pulvinar complex in nonprimate species: mice, rats, rabbits, cats, and tree shrews) (Casanova and Molotchnikoff 1990). ...
Sensorimotor cortical areas contain eye position information thought to ensure perceptual stability across saccades and underlie spatial transformations supporting goal-directed actions. One pathway by which eye position signals could be relayed to and across cortical areas is via the dorsal pulvinar. Several studies demonstrated saccade-related activity in the dorsal pulvinar and we have recently shown that many neurons exhibit post-saccadic spatial preference. In addition, dorsal pulvinar lesions lead to gaze-holding deficits expressed as nystagmus or ipsilesional gaze bias, prompting us to investigate the effects of eye position. We tested three starting eye positions (-15°/0°/15°) in monkeys performing a visually-cued memory saccade task. We found two main types of gaze dependence. First, ~50% of neurons showed dependence on static gaze direction during initial and post-saccadic fixation, and might be signaling the position of the eyes in the orbit, or coding foveal targets in a head/body/world-centered reference frame. The population-derived eye position signal lagged behind the saccade. Second, many neurons showed a combination of eye-centered and gaze-dependent modulation of visual, memory and saccadic responses to a peripheral target. A small subset showed effects consistent with eye position-dependent gain modulation. Analysis of reference frames across task epochs from visual cue to post-saccadic fixation indicated a transition from predominantly eye-centered encoding to representation of final gaze or foveated locations in non-retinocentric coordinates. These results show that dorsal pulvinar neurons carry information about eye position, which could contribute to steady gaze during postural changes and to reference frame transformations for visually-guided eye and limb movements.
... Although the LP receives inputs from subcortical areas (Chalupa et al. 1983), the model considered that the external current for the thalamic neurons depended only on cortical inputs as shown by empirical data (Bender 1983). A thalamic neuron (i, A, lp) received current inputs simultaneously from the four cortical areas. ...
The pulvinar is the largest extrageniculate visual nucleus in mammals. Given its extensive reciprocal connectivity with the visual cortex, it allows the cortico-thalamocortical transfer of visual information. Nonetheless, knowledge of the nature of the pulvinar inputs to the cortex remains elusive. We investigated the impact of silencing the pulvinar on the contrast response function of neurons in 2 distinct hierarchical cortical areas in the cat (areas 17 and 21a). Pulvinar inactivation altered the response gain in both areas, but with larger changes observed in area 21a. A theoretical model was proposed, simulating the pulvinar contribution to cortical contrast responses by modifying the excitation-inhibition balanced state of neurons across the cortical hierarchy. Our experimental and theoretical data showed that the pulvinar exerts a greater modulatory influence on neuronal activity in area 21a than in the primary visual cortex, indicating that the pulvinar impact on cortical visual neurons varies along the cortical hierarchy.
... The functional contribution of projections from SC is more studied in the ventral pulvinar, where the effects of SC perturbation or lesions have been assessed in several studies. Specifically, extensive lesions of SC caused only little effect on visual responses in the ventral pulvinar, as compared to striate cortex lesions (Bender, 1983). In rabbits, however, the inactivation of SC led to a strong attenuation of responses in lateral posterior nucleus (which is a part of the LP-pulvinar complex in non-primate species: mice, rats, rabbits, cats, and tree shrews) (Casanova and Molotchnikoff, 1990). ...
Most sensorimotor cortical areas contain eye position information thought to ensure perceptual stability across saccades and underlie spatial transformations supporting goal-directed actions. One pathway by which eye position signals could be relayed to and across cortical areas is via the dorsal pulvinar. Several studies demonstrated saccade-related activity in the dorsal pulvinar and we have recently shown that many neurons exhibit post-saccadic spatial preference long after the saccade execution. In addition, dorsal pulvinar lesions lead to gaze-holding deficits expressed as nystagmus or ipsilesional gaze bias, prompting us to investigate the effects of eye position. We tested three starting eye positions (−15°/0°/15°) in monkeys performing a visually-cued memory saccade task. We found two main types of gaze dependence. First, ∼50% of neurons showed an effect of static gaze direction during initial and post-saccadic fixation. Eccentric gaze preference was more common than straight ahead. Some of these neurons were not visually-responsive and might be primarily signaling the position of the eyes in the orbit, or coding foveal targets in a head/body/world-centered reference frame. Second, many neurons showed a combination of eye-centered and gaze-dependent modulation of visual, memory and saccadic responses to a peripheral target. A small subset showed effects consistent with eye position-dependent gain modulation. Analysis of reference frames across task epochs from visual cue to post-saccadic target fixation indicated a transition from predominantly eye-centered encoding to representation of final gaze or foveated locations in non-retinocentric coordinates. These results show that dorsal pulvinar neurons carry information about eye position, which could contribute to steady gaze during postural changes and to reference frame transformations for visually-guided eye and limb movements.
New & Noteworthy
Work on the pulvinar focused on eye-centered visuospatial representations, but position of the eyes in the orbit is also an important factor that needs to be taken into account during spatial orienting and goal-directed reaching. Here we show that dorsal pulvinar neurons are influenced by eye position. Gaze direction modulated ongoing firing during stable fixation, as well as visual and saccade responses to peripheral targets, suggesting involvement of the dorsal pulvinar in spatial coordinate transformations.
... In primates, the ''secondary'' visual pathway running through SC and pulvinar has traditionally been thought to play a modulatory role in visual processing, potentially relaying saccade-modulated visual signals (Berman and Wurtz, 2011;Berman et al., 2017). Previous studies disagreed whether SC input could drive receptive field properties in pulvinar neurons (Bender, 1983;Casanova and Molotchnikoff, 1990), perhaps depending on species and/or where in the pulvinar recordings were made. Our data show that pLP neurons are tuned similarly to their input from SC. ...
Higher-order thalamic nuclei, such as the visual pulvinar, play essential roles in cortical function by connecting functionally related cortical and subcortical brain regions. A coherent framework describing pulvinar function remains elusive because of its anatomical complexity and involvement in diverse cognitive processes. We combined large-scale anatomical circuit mapping with high-density electrophysiological recordings to dissect a homolog of the pulvinar in mice, the lateral posterior thalamic nucleus (LP). We define three broad LP subregions based on correspondence between connectivity and functional properties. These subregions form corticothalamic loops biased toward ventral or dorsal stream cortical areas and contain separate representations of visual space. Silencing the visual cortex or superior colliculus revealed that they drive visual tuning properties in separate LP subregions. Thus, by specifying the driving input sources, functional properties, and downstream targets of LP circuits, our data provide a roadmap for understanding the mechanisms of higher-order thalamic function in vision.
... The pulvinar receives a massive afferent input from V1 (1,9), and its response to visual stimuli depends on V1 (1,19). Because silencing of V1 has a minor effect on POR activity, the pulvinar might seem a poor candidate for relaying visual activity to POR. ...
Another primary visual cortex
Most functional studies in the visual system have focused on the cortical representation of the geniculo-striate pathway that links the retina to the cortex. The parallel collicular pathway is believed to sparsely project throughout the visual cortex and have a modulatory role on cortical responses to visual stimuli. Beltramo and Scanziani found a visual cortical area that is entirely dedicated to the superior colliculus. This area can discriminate moving visual stimuli that the “classical” primary visual cortex cannot. Thus, the superior colliculus, a phylogenetically ancient structure, has its own projection in neocortex that provides this area with exquisite feature-detection abilities not found in the classical primary visual cortex.
Science , this issue p. 64
... This projection comes from a cell type that is distinct from the dLGNprojecting sSC neurons 39 . It could be a driving input 40 , but SC lesions have little impact on activity in the monkey pulvinar 41 . This is species specific or dependent on the subarea of pulvinar. ...
The largest targets of retinal input in mammals are the dorsal lateral geniculate nucleus (dLGN), a relay to the primary visual cortex (V1), and the superior colliculus. V1 innervates and influences the superior colliculus. Here, we find that, in turn, superior colliculus modulates responses in mouse V1. Optogenetically inhibiting the superior colliculus reduces responses in V1 to optimally sized stimuli. Superior colliculus could influence V1 via its strong projection to the lateral posterior nucleus (LP/Pulvinar) or its weaker projection to the dLGN. Inhibiting superior colliculus strongly reduces activity in LP. Pharmacologically silencing LP itself, however, does not remove collicular modulation of V1. The modulation is instead due to a collicular gain modulation of the dLGN. Surround suppression operating in V1 explains the different effects for differently sized stimuli. Computations of visual saliency in the superior colliculus can thus influence tuning in the visual cortex via a tectogeniculate pathway.
... In primates, the ''secondary'' visual pathway running through SC and pulvinar has traditionally been thought to play a modulatory role in visual processing, potentially relaying saccade-modulated visual signals (Berman and Wurtz, 2011;Berman et al., 2017). Previous studies disagreed whether SC input could drive receptive field properties in pulvinar neurons (Bender, 1983;Casanova and Molotchnikoff, 1990), perhaps depending on species and/or where in the pulvinar recordings were made. Our data show that pLP neurons are tuned similarly to their input from SC. ...
Higher-order thalamic nuclei, such as the visual pulvinar, play essential roles in shaping cortical dynamics and connecting functionally-related cortical and subcortical brain regions. A coherent framework describing pulvinar function remains elusive due to its anatomical complexity, involvement in diverse cognitive processes, and the limited experimental tools available in many species. We combined large-scale anatomical circuit mapping with high-density electrophysiological recordings to dissect a homolog of pulvinar in mice, the lateral posterior nucleus (LP). We define three LP subregions based on correspondence between connectivity and functional properties. These subregions form parallel corticothalamic loops and contain separate representations of visual space. Silencing visual cortex or the superior colliculus revealed that these input sources drive activity and shape visual tuning in separate LP subregions. By specifying the information carried by distinct circuits through LP and identifying their downstream targets, our data provide a roadmap for understanding pulvinar function in visual processing and behavior.
... Inferior pulvinar neurons also possess a range of speed-sensitivities, mostly preferring slower motion under 32˚/s [54,55], not dissimilar to V1 responses. It is suggested that those responses may arise from striate cortex inputs [56], and it was interesting that blindsight-negative patients showed evidence of peripheral V1 activation, making this a possible source of input. Macaque LGN neurons also demonstrate a range of speed preferences, particularly in magnocellular neurons, but most prefer somewhat faster motion [57]. ...
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 pulvinar complex, as a whole, has both modulatory and driving influences, but each nucleus within the pulvinar likely has a predominantly driving influence, or a predominantly modulatory influence on cortex. PIp and PIcm appear to have predominantly driving roles in temporal cortex, while PIm (in the mature brain), PIcl, and PL all appear to have modulatory roles (Bender, 1983;Sherman & Guillery 2006;Rovo, Ulbert, & Acsady, 2012;Balaram et al., 2013). ...
In this review, we outline the history of our current understanding of the organization of the pulvinar complex of mammals, including more recent evidence from our own studies of both New and Old World monkeys, prosimian galagos, and close relatives of primates, including tree shrews and rodents. Based on cumulative evidence, we provide insights into the possible evolution of the visual pulvinar complex, as well as the possible co-evolution of the inferior pulvinar nuclei and temporal cortical visual areas within the MT complex. This article is protected by copyright. All rights reserved.
... As discussed above, some pulvinar cells demonstrably act as a relay between the colliculus and area V5 Wurtz, 2010, 2011) -but this may not be the dominant mode of function. Inputs from the midbrain are outnumbered by those from cortex, and the effects of disabling these two sources are asymmetric: lesions of the colliculus produced minor delays in responsivity, in a minority of cells; lesions of V1 rendered pulvinar cells unresponsive, unless tested 3 weeks postoperatively, when a fraction of cells with collicular visual characteristics were recorded (Bender, 1983). There is also a potentially intriguing anatomical observation to be made. ...
Introduction
The term pulvinar derives from the Latin for a cushion. Being the thalamic nucleus situated adjacent to the Lateral Geniculate (‘knee-like’) nucleus (LGN) the term is quite apt, though the humour may not have been intentional. The LGN and pulvinar constitute the twin thalamic elements of the visual system, but they differ significantly in structure and connectivity. The LGN has significant connections external to its primary cortical target (area V1), but the scope of pulvinocortical circuitry is far more extensive. In fact there is no known region of ipsilateral visual cortex that fails to interact with the pulvinar, and parts of somatosensory, auditory, cingulate and frontal cortices are also connected to it. Also unlike the LGN, the pulvinar receives only a very sparse retinal input, and lacks the layered structure associated with segregated ocular inputs and monocular response properties. Instead, it appears that a specific subset of cortical inputs to the pulvinar mimics the role of retinal afferents to the LGN – both are known as ‘primary afferents’. On this basis, the pulvinar is classified as a higher-order thalamic relay (and the LGN is termed a first-order relay). It therefore follows that the prime purpose of the pulvinar is to operate a set of cortico-thalamo-cortical (CTC) loops, for the pulvinar has no greater anatomical output than its return projections to the cortex.
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... Lesions to SC in anesthetized macaques with V1 lesions silenced MT responses (Rodman et al., 1990), suggesting that the retinocollicular pathway is necessary. However, the collicular pathway to extrastriate cortex passes through the inferior pulvinar (Berman et al., 2009;Berman and Wurtz, 2010), which was found to be largely unresponsive inside the lesion projection zones, following V1 lesions in adult macaques (Bender, 1983), although a few cells regained visual responses greater than 4 weeks post-lesion. More recent studies have shown that in awake-behaving macaques with V1 lesions, temporary LGN inactivation removes all residual behavioral effects of blindsight (Schmid et al., 2011), demonstrating that the retinogeniculate pathway is necessary for mediating the visual behaviors of blindsight. ...
For nearly a century it has been observed that some residual visually guided behavior can persist after damage to the primary visual cortex (V1) in primates. The age at which damage to V1 occurs leads to different outcomes, with V1 lesions in infancy allowing better preservation of visual faculties in comparison with those incurred in adulthood. While adult V1 lesions may still allow retention of some limited visual abilities, these are subconscious - a characteristic that has led to this form of residual vision being referred to as blindsight. The neural basis of blindsight has been of great interest to the neuroscience community, with particular focus on understanding the contributions of the different subcortical pathways and cortical areas that may underlie this phenomenon. More recently, research has started to address which forms of neural plasticity occur following V1 lesions at different ages, including work using marmoset monkeys. The relatively rapid postnatal development of this species, allied to the lissencephalic brains and well-characterized visual cortex provide significant technical advantages, which allow controlled experiments exploring visual function in the absence of V1. This article is protected by copyright. All rights reserved.
... It is this other thalamus -higher order nuclei plus extended intralaminar complex -that is the target of the cortical layer 5 pyramidal cell projection, justifying a collective designation for this large set of thalamic nuclei. The layer 5 projection has "driving" properties, and crucially determines higher order thalamic receptive fields (Bender 1983;Diamond et al. 1992). Figure 5. Schematic depiction of connective relations between cortex, thalamus and colliculus discussed in the text. ...
... Pessoa and Adolphs (2010) summarize physiological data suggesting that the subcortical pathway does not process threats more quickly than the cortical pathway. In addition, SC lesions have little impact upon visual activity in the monkey pulvinar nucleus (Bender, 1983), questioning the functional connectivity between the two brain areas. While the SC projects primarily to the inferior pulvinar nucleus, the output from this area is directed to the cortex and not the amygdala (reviewed by Pessoa and Adolphs, 2010). ...
Although there is general agreement that the central nucleus of the amygdala (CeA) is critical for triggering the neuroendocrine response to visual threats, there is uncertainty about the role of subcortical visual pathways in this process. Primates in general appear to depend less on subcortical visual pathways than other mammals. Yet, imaging studies continue to indicate a role for the superior colliculus and pulvinar nucleus in fear activation, despite disconnects in how these brain structures communicate not only with each other but with the amygdala. Studies in fish and amphibians suggest that the neuroendocrine response to visual threats has remained relatively unchanged for hundreds of millions of years, yet there are still significant data gaps with respect to how visual information is relayed to telencephalic areas homologous to the CeA, particularly in fish. In fact ray finned fishes may have evolved an entirely different mechanism for relaying visual information to the telencephalon. In part because they lack a pathway homologous to the lateral geniculate-striate cortex pathway of mammals, amphibians continue to be an excellent model for studying how stress hormones in turn modulate fear activating visual pathways. Glucocorticoids, melanocortin peptides, and CRF all appear to play some role in modulating sensorimotor processing in the optic tectum. These observations, coupled with data showing control of the hypothalamus-pituitary-adrenal axis by the superior colliculus, suggest a fear/stress/anxiety neuroendocrine circuit that begins with first order synapses in subcortical visual pathways. Thus, comparative studies shed light not only on how fear triggering visual pathways came to be, but how hormones released as a result of this activation modulate these pathways.
... This pathway is prominent in mammals and most studied in rodents [33]. Yet in adult primates even the inferior pulvinar is driven primarily by the visual cortex, as demonstrated in a seminal electrophysiological study [34]. Removal of V1 led to the near [ 8 _ T D $ D I F F ] abolition of activity in the pulvinar with a few residual responses attributed to the retinocollopulvinar visual pathway [35], although there is some uncertainty regarding the precise recording locations in this early work. ...
The pulvinar is the largest thalamic nucleus in primates and one of the most mysterious. Endeavors to understand its role in vision have focused on its abundant connections with the visual cortex. While its connectivity mapping in the cortex displays a broad topographic organization, its projections are also marked by considerable convergence and divergence. As a result, the pulvinar is often regarded as a central forebrain hub. Moreover, new evidence suggests that its comparatively modest input from structures such as the retina and superior colliculus may critically shape the functional organization of the visual cortex, particularly during early development. Here we review recent studies that cast fresh light on how the many convergent pathways through the pulvinar contribute to visual cognition.
... The cryoblockade or lesion of area 17 strongly decreases visual responses in a subset of LPl neurons (Casanova et al. 1997). Similarly in primates, the removal of primary visual cortex (V1) eliminates visual responses for the vast majority of pulvinar neurons (Bender 1983). Thus, given the functional significance of striate input on the LPl neurons, one could expect that their RF spatial structure be mainly sculpted by signals from area 17 complex cells. ...
The pulvinar is the largest extrageniculate thalamic visual nucleus in mammals. It establishes reciprocal connections with virtually all visual cortices and likely plays a role in transthalamic cortico-cortical communication. In cats, the lateral posterior nucleus (LP) of the LP-pulvinar complex can be subdivided in two subregions, the lateral (LPl) and medial (LPm) parts, which receive a predominant input from the striate cortex and the superior colliculus, respectively. Here, we revisit the receptive field structure of LPl and LPm cells in anesthetized cats, by determining their spatiotemporal profiles through reverse correlation analysis following sparse noise stimulation. Our data reveal the existence of previously unidentified receptive field profiles in the LP nucleus both in space and time domains. While some cells responded to only one stimulus polarity, the majority of neurons had receptive fields comprised of bright- and dark-responsive subfields. For these neurons, dark subfields' size was larger than that of bright subfields. All types of receptive field's spatial organization were found in both LPl and LPm subregions, ranging from totally overlapped to segregated bright and dark subfields. In the time domain, a large spectrum of activity overlap was found, from cells with temporally coinciding subfield activity to neurons with distinct, time-dissociated subfield peak activity windows. We also found LP neurons with space-time inseparable receptive fields and neurons with multiple activity windows. Finally, no outstanding difference exists between receptive field spatiotemporal profiles within the two LP subdivisions, suggesting a high integration of cortical and subcortical inputs within the LP-pulvinar complex.
Copyright © 2013, Journal of Neurophysiology.
... The very first anatomical studies of the pulvinar have been conducted in the macaque monkey of which the pulvinar has been divided on the basis of cytoarchitectonic criteria into four parts: the lateral, medial, inferior, and oral pulvinar nuclei. The lateral and inferior nuclei have been found to be retinotopically organized (Bender, 1981a(Bender, ,b, 1982. Also anatomical studies in mammals revealed that the pulvinar receives inputs from subdivisions of visual cortex and back projects to these Romanski et al., 1997;Casanova et al., 2001;Guillery and Sherman, 2002a/b;Sherman and Guillery, 2002;Shipp et al., 1998;Shipp, 2001Shipp, , 2003Shipp, , 2004Sherman, 2005;Kaas and Lyon, 2007) via long-range interneurons, while visuo-somatomotor connections via the pulvinar have been suggested a long time ago (Shipp et al., 1995;Shipp and Zeki, 1998). ...
... For example, it is possible that direct koniocellular LGN to hMT+ inputs (Sincich et al., 2004) modulate spurious motion signals that arise from microsaccades or other sources. Although there is direct tectopulvinar input to hMT+ that bypasses V1, it is not likely that microsaccadic suppression is driven by this bottom-up pathway, because the motion and other visual tuning properties of pulvinar nucleus cells appear to be driven cortically rather than via bottom-up input from superior colliculus cells (Bender, 1983). Indeed, tectal cells are not orientation or direction selective (Cynader and Berman, 1972), making it unlikely that a bottom-up motion signal reaches hMT+ via the tectopulvinar pathway at all. ...
Microsaccades are small, conjugate, involuntary eye-movements made while voluntarily fixating, which play a role in minimizing perceptual fading. The goal of this research was to determine the neural correlates of microsaccade occurrence in early visual areas of cortex using fMRI. This is an important issue for fMRI researchers because so far no laboratory has controlled for the possibility that microsaccade events, rates or magnitudes are correlated with experimental conditions. If microsaccades are found to generate BOLD signal changes in the cortex, many past fMRI results may have arisen as a result of this confound. Methods: We recorded both involuntary microsaccades, and voluntary saccades from one eye in the spatiotemporal domain of microsaccades using a Limbus infrared eyetracker (1000Hz sampling), while collecting fMRI data in a mixed, event-related/block design (3T Siemens Allegra scanner, TR=402ms, 11 slices along calcarine, TE=30ms, FA=35°, 800 volumes, n=6, 6–8 runs per subject). In two blocks per run subjects executed small voluntary saccades (0.16°, 12 pseudorandom events per block), maintained fixation on a small point jumping left and right. A long fixation-only period separated these blocks. The fixation point was centered on a 1° wide horizontal white band laid over a polar grating. Retinotopic mapping used standard methods (TR=2000ms, TE=30ms, FA=90°, 30 slices, 152 volumes). Results: BOLD signal is greater in early visual areas for very small voluntary saccades, relative to fixation epochs, which are as small as true microsaccades. An event-related deconvolution analysis of true microsaccades that occurred during fixation-only epochs revealed upward modulation of the BOLD signal in V1 and V2 after the occurrence of a microsaccade. We conclude that, to the extent that microsaccades may be correlated with experimental conditions, the results of fMRI studies may arise because of microsaccades, and not the experimental variables under consideration, forcing a reevaluation of many past fMRI results.
... VGLUT distributions in the lateral and inferior pulvinar highlighted the heterogeneity of afferent and efferent projections in these nuclei, but were still instrumental in defining subdivisions in the inferior pulvinar. Diffuse VGLUT1 terminal labeling across the lateral and inferior pulvinar that resembled patterns of corticopulvinar terminations in macaques (Campos-Ortega and Hayhow, 1972;Maunsell and Van Essen, 1983;Ogren and Hendrickson, 1979) supports the conclusion that these structures are dominated by inputs from visual cortical areas and not subcortical structures (Adams et al, 2000;Bender, 1983;Shipp 2001;Van Essen 2005). Clear exceptions to this inference are the posterior and central medial nuclei of the inferior pulvinar, which primarily receive inputs from the superior colliculus (see above) and showed dense distributions of VGLUT2 positive terminals instead. ...
Glutamate is the primary neurotransmitter utilized by the mammalian visual system for excitatory neurotransmission. The sequestration of glutamate into synaptic vesicles, and the subsequent transport of filled vesicles to the presynaptic terminal membrane, is regulated by a family of proteins known as vesicular glutamate transporters (VGLUTs). Two VGLUT proteins, VGLUT1 and VGLUT2, characterize distinct sets of glutamatergic projections between visual structures in rodents and prosimian primates, yet little is known about their distributions in the visual system of anthropoid primates. We have examined the mRNA and protein expression patterns of VGLUT1 and VGLUT2 in the visual system of macaque monkeys, an Old World anthropoid primate, in order to determine their relative distributions in the superior colliculus, lateral geniculate nucleus, pulvinar complex, V1 and V2. Distinct expression patterns for both VGLUT1 and VGLUT2 identified architectonic boundaries in all structures, as well as anatomical subdivisions of the superior colliculus, pulvinar complex, and V1. These results suggest that VGLUT1 and VGLUT2 clearly identify regions of glutamatergic input in visual structures, and may identify common architectonic features of visual areas and nuclei across the primate radiation. Additionally, we find that VGLUT1 and VGLUT2 characterize distinct subsets of glutamatergic projections in the macaque visual system; VGLUT2 predominates in driving or feedforward projections from lower order to higher order visual structures while VGLUT1 predominates in modulatory or feedback projections from higher order to lower order visual structures. The distribution of these two proteins suggests that VGLUT1 and VGLUT2 may identify class 1 and class 2 type glutamatergic projections within the primate visual system (Sherman and Guillery, 2006).
To examine the biological building blocks of thought and action, we created biologically realistic local circuits based on detailed well-cited physiological and anatomical characteristics. These biomimetic circuits were then integrated into a large-scale model of cortical-striatal interactions for category learning. The model was not trained on, but nonetheless displayed properties similar to, neurophysiological recordings from non-human primates (NHPs) performing the same task. The model had learning curves similar to the NHPs. It showed how synaptic modifications could induce changes in spiking and synchrony in the brain. The model even made novel predictions that were subsequently found in the brain, including "bad-idea neurons" that signalled impending incorrect choices after learning. This demonstrates how key computational principles can be discovered by modeling local circuitry that mimics the brain.
In prosimian galagos, the posterior parietal cortex (PPC) is subdivided into a number of functional domains where long‐train intracortical microstimulation evoked different types of complex movements. Here, we placed anatomical tracers in multiple locations of PPC to reveal the origins and targets of thalamic connections of four PPC domains for different types of hindlimb, forelimb, or face movements. Thalamic connections of all four domains included nuclei of the motor thalamus, ventral anterior and ventral lateral nuclei, as well as parts of the sensory thalamus, the anterior pulvinar, posterior and ventral posterior superior nuclei, consistent with the sensorimotor functions of PPC domains. PPC domains also projected to the thalamic reticular nucleus in a somatotopic pattern. Quantitative differences in the distributions of labeled neurons in thalamic nuclei suggested that connectional patterns of these domains differed from each other. The posterior parietal cortex (PPC) of galagos contains a series of domains where electrical stimulation evokes different types of complex movements. The medial domains have more connections with the motor thalamus, whereas the lateral domains connect more densely with the posterior thalamus that involves in somatosensory processing.
Some patients with damage to the primary visual cortex (V1) exhibit visuomotor ability, despite loss of visual awareness, a phenomenon termed “blindsight”. We review a series of studies conducted mainly in our laboratory on macaque monkeys with unilateral V1 lesioning to reveal the neural pathways underlying visuomotor transformation and the cognitive capabilities retained in blindsight. After lesioning, it takes several weeks for the recovery of visually guided saccades toward the lesion-affected visual field. In addition to the lateral geniculate nucleus, the pathway from the superior colliculus to the pulvinar participates in visuomotor processing in blindsight. At the cortical level, bilateral lateral intraparietal regions become critically involved in the saccade control. These results suggest that the visual circuits experience drastic changes while the monkey acquires blindsight. In these animals, analysis based on signal detection theory adapted to behavior in the “Yes-No” task indicates reduced sensitivity to visual targets, suggesting that visual awareness is impaired. Saccades become less accurate, decisions become less deliberate, and some forms of bottom-up attention are impaired. However, a variety of cognitive functions are retained such as saliency detection during free viewing, top-down attention, short-term spatial memory, and associative learning. These observations indicate that blindsight is not a low-level sensory-motor response, but the residual visual inputs can access these cognitive capabilities. Based on these results we suggest that the macaque model of blindsight replicates type II blindsight patients who experience some “feeling” of objects, which guides cognitive capabilities that we naïvely think are not possible without phenomenal consciousness.
Two main types of cortical terminals have been identified in the cat thalamus. Large (type II) have been proposed to drive the response properties of thalamic cells while smaller (type I) are believed to modulate those properties. Among the cat’s visual cortical areas, the anterior ectosylvian visual area (AEV) is considered as one of the highest areas in the hierarchical organization of the visual system. Whereas the connections from the AEV to the thalamus have been recognized, their nature (type I or II) is presently not known. In this study, we assessed and compared the relative contribution of type I and type II inputs to thalamic nuclei originating from the AEV. The anterograde tracer BDA was injected in the AEV of five animals. Results show that (1) both type I and II terminals from AEV are present in the Lateral Posterior- Pulvinar complex, the lateral median suprageniculate complex and the medial and dorsal geniculate nuclei (2) type I terminals significantly outnumber the type II terminals in almost all nuclei studied. Our results indicate that neurons in the AEV are more likely to modulate response properties in the thalamus rather than to determine basic organization of receptive fields of thalamic cells.
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.
Comprised of at least five distinct nuclei, the pulvinar complex of primates includes two large visually driven nuclei; one in the dorsal (lateral) pulvinar and one in the ventral (inferior) pulvinar, that contain similar retinotopic representations of the contralateral visual hemifield. Both nuclei also appear to have similar connections with areas of visual cortex. Here we determined the cortical connections of these two nuclei in galagos, members of the stepsirrhine primate radiation, to see if the nuclei differed in ways that could support differences in function. Injections of different retrograde tracers in each nucleus produced similar patterns of labeled neurons, predominately in layer 6 of V1, V2, V3, MT, regions of temporal cortex, and other visual areas. More complete labeling of neurons with a modified rabies virus identified these neurons as pyramidal cells with apical dendrites extending into superficial cortical layers. Importantly, the distributions of cortical neurons projecting to each of the two nuclei were highly overlapping, but formed separate populations. Sparse populations of double labeled neurons were found in both V1 and V2 but were very low in number (<0.1%). Finally, the labeled cortical neurons were predominately in layer 6 and layer 5 neurons were labeled only in extrastriate areas. Terminations of pulvinar projections to area 17 was largely in superficial cortical layers, especially layer 1.
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Corticopulvinar axons were anterogradely labeled by Phaseolus vulgaris-leucoagglutinin injections in the occipitotemporal cortex of the macaque to determine quantitative parameters of divergence and convergence, arbor size and shape, and distribution of terminal specializations. Forty individual axons were analyzed by serial section reconstruction and divided into two major groups. The majority of axons have numerous (typically 500–1,000) small, spinous endings (boutons terminaux). These axons have terminal fields that are beam-like or elongated (E, corresponding to classical type 1) and highly divergent (1.0–3.0 mm). These frequently innervate several of the traditionally designated pulvinar subdivisions; namely inferior pulvinar (PI) and the ventral part of interal pulvinar (PL); medial pulvinar (PM) and dorsal PL, and (one axon) PM, dorsal PL, and PI. Some axons, however (R or round, corresponding to classical type 2), have a small number (typically 70–160) of primarily large, beaded endings (boutons en passant), which concentrate in sharply delimited, round arbors (diameters 100–125 μm). R axons appear to be larger caliber than E axons (1.0–1.5 μm vs. 0.5–1.0 μm, respectively). These differences in phenotype are probably associated with distinct types of projection neurons. In visual areas, corticopulvinar terminations are reported to originate from pyramidal cell subpopulations in layer 5. Indirect evidence, presented here, suggests that the more numerous medium-sized neurons give rise to E axons, and the sparser giant pyramids give rise to R corticopulvinar axons. If this is correct, corticopulvinar connectivity may be involved in multiple transformations. Spatially, axons of giant neurons (with basal dendrites that collect intracortically from a disc-like area, about 1.0 mm in diameter) converge onto a small number of pulvinar neurons. Axons of medium neurons (with basal dendrites that occupy a small intracortical disc, about 0.3 mm in diameter) diverge over 1.0–3.0 mm in the pulvinar and may form many contacts. Giant neurons, although numerically few in relation to medium pyramids (1 or 2: 50?), are likely to have distinctive membrane properties (functionally equivalent to bursting neurons?). Their larger boutons and axon caliber may be associated with a faster transmission that compensates for their small numbers. In primates, the E and R duality does not characterize cortical projections to the caudate, lateral geniculate nucleus, pons, or superior colliculus and thus may be essentially linked to pulvinar-specific processes.
Glutamatergic pathways in thalamus and cortex are divided into two distinct classes: driver, which carries the main information between cells, and modulator, which modifies how driver inputs function. Identifying driver inputs helps to reveal functional computational circuits, and one set of such circuits identified by this approach are cortico-thalamo-cortical (or transthalamic corticocortical) circuits. This, in turn, leads to the conclusion that there are two types of thalamic relay: first order nuclei (such as the lateral geniculate nucleus) that relay driver input from a subcortical source (i.e., retina), and higher order nuclei (such as the pulvinar) which are involved in these transthalamic pathways by relaying driver input from layer 5 of one cortical area to another. This thalamic division is also seen in other sensory pathways and beyond these so that most of thalamus by volume consists of higher-order relays. Many, and perhaps all, direct driver connections between cortical areas are paralleled by an indirect cortico-thalamo-cortical (transthalamic) driver route involving higher order thalamic relays. Such thalamic relays represent a heretofore unappreciated role in cortical functioning, and this assessment challenges and extends conventional views regarding both the role of thalamus and mechanisms of corticocortical communication. Finally, many and perhaps the vast majority of driver inputs relayed through thalamus arrive via branching axons, with extrathalamic targets often being subcortical motor centers. This raises the possibility that inputs relayed by thalamus to cortex also serve as efference copies, and this may represent an important feature of information relayed up the cortical hierarchy via transthalamic circuits. © 2017 American Physiological Society. Compr Physiol 7:713-739, 2017.
The lateral geniculate body is the major processing nucleus for retinal information; however, in 1961 Altman and Carpenter drew attention to the thalamic projection from the superior colliculi; these bodies receive a powerful retinal projection, so that this collicular projection reveals an indirect access of visual information to the cerebral cortex. The target-areas of the ascending collicular projections are mainly within the pulvinar posterior system of the thalamus (PUL-PO), which, in turn, receives a strong projection from the visual cortex. Besides the colliculus, the adjacent pretectal region contains nuclei receiving retinal input; thus the circuitry for this subsidary processing system may be indicated crudely by Fig. 23.1. We shall see that the cortical influence on the colliculi is profound, so that their receptive-field characteristics become very similar to those of certain cortical cells.
Several challenges to current views of thalamocortical processing are offered here. Glutamatergic pathways in thalamus and cortex are divided into two distinct classes: driver and modulator. We suggest that driver inputs are the main conduits of information and that modulator inputs modify how driver inputs are processed. Different driver sources reveal two types of thalamic relays: first order relays receive subcortical driver input (for example, retinal input to the lateral geniculate nucleus), whereas higher order relays (for example, pulvinar) receive driver input from layer 5 of cortex and participate in cortico-thalamo-cortical (or transthalamic) circuits. These transthalamic circuits represent an unappreciated aspect of cortical functioning, which I discuss here. Direct corticocortical connections are often paralleled by transthalamic ones. Furthermore, driver inputs to thalamus, both first and higher order, typically arrive via branching axons, and the transthalamic branch often innervates subcortical motor centers, leading to the suggestion that these inputs to thalamus serve as efference copies.
Corticopulvinar connections consist of at least two morphologically distinct subpopulations. In one subgroup (E, type 1), axons have an "elongated" terminal field and thin, spinous terminations; in the other (R, type 2), axons have a small, round arbor and large, beaded terminations. Previous work (Rockland, 1996) indicates that E-type axons from several occipitotemporal areas branch extensively within and sometimes between pulvinar subdivisions, but that R-type axons tend to have spatially delimited arbors. The present report is a further investigation of R-type axons from areas VI and MT and was initiated to test the generality of the previous findings. There are four :main results: 1) By serial section reconstruction of anterogradely labeled axons, 10 of 25 axons originating in area V1 had two or three spatially separate arbors (8 and 2 axons, respectively). Sixteen axons analyzed from area MT, however, all had single arbors, although the arbors were often formed by the convergence of widely separate branches. 2) Multiple (at least 2-5) R-type corticopulvinar axons, from V1 or from MT, can converge in a single focus. 3) R-type axons originating from both areas V1 and MT can branch to other structures; namely, the superior colliculus, the pretectal area, and/or the reticular nucleus of the thalamus. 4) Finally, corticopulvinar terminations from area V1 are predominantly R-type, whereas those from MT are more predominantly E-type. These results thus provide additional evidence of the special relationship of area V1 to the pulvinar. They also emphasize that the idea of corticopulvinocortical "feedback loops," although convenient as a shorthand nomenclature, does not adequately convey the full complexity of the system. (C) 1998 Wiley-Liss, Inc.
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 ideas concerning the role of area 17 in the transfer of visual information to the rest of the cerebral cortex have for a long time been influenced by the results of behavioral studies of primates following cortical lesions. Since the last century it has been known that lesions of area 17 lead to blindness in humans (for a review see Weiskrantz, 1986, and Rizzo, this volume). This critical role of area 17 in vision was used in the beginning of the 20th century by Inouye in Japan and Holmes in Great Britain to map the representation of the visual field in area 17 of humans by delimiting the extents of scotomata resulting from focal lesions in area 17 of wounded soldiers. In 1942, the results of an extensive study by Klüver of monkeys with cortical lesions seemed to leave little doubt that, for this species as well, area 17 is necessary for any kind of vision beyond a simple discrimination between light and dark. Rudimentary sensitivity to light had also been noted to persist in humans with lesions of area 17 by Holmes (1918) and Riddoch (1917). Interestingly, this last author noted a weak residual sensitivity to moving targets, but no perception of stationary objects.
Among the many unique features of the auditory system one of the more notable is the large number of processing centers (cell groups) interposed between the system’s periphery and its cortex. Our main purpose in this chapter is to build upon the first 2 volumes in this series (Popper and Fay 1992; Webster et al. 1992) by highlighting progress made over the last decade in understanding these structures of the auditory pathway, especially when this information can be related to functional hypotheses about particular cell groups or neural circuits.
Unlabelled:
The primary visual cortex (V1) receives its main thalamic drive from the dorsal lateral geniculate nucleus (dLGN) through synaptic contacts terminating primarily in cortical layer IV. In contrast, the projections from the pulvinar nucleus to the cortex are less clearly defined. The pulvinar projects predominantly to layer I in V1, and layer IV in extrastriate areas. These projection patterns suggest that the pulvinar nucleus most strongly influences (drives) activity in cortical areas beyond V1. Should this hypothesis be true, one would expect the spatiotemporal responses evoked by pulvinar activation to be different in V1 and extrastriate areas, reflecting the different connectivity patterns. We investigated this issue by analyzing the spatiotemporal dynamics of cortical visual areas' activity following thalamic electrical microstimulation in tree shrews, using optical imaging and voltage-sensitive dyes. As expected, electrical stimulation of the dLGN induced fast and local responses in V1, as well as in extrastriate and contralateral cortical areas. In contrast, electrical stimulation of the pulvinar induced fast and local responses in extrastriate areas, followed by weak and diffuse activation in V1 and contralateral cortical areas. This study highlights spatiotemporal cortical activation characteristics induced by stimulation of first (dLGN) and high-order (pulvinar) thalamic nuclei.
Significance statement:
The pulvinar nucleus represents the main extrageniculate thalamic visual structure in higher-order mammals, but its exact role remains enigmatic. The pulvinar receive prominent inputs from virtually all visual cortical areas. Cortico-thalamo-cortical pathways through the pulvinar nuclei may then provide a complementary route for corticocortical information flow. One step toward the understanding of the role of transthalamic corticocortical pathways is to determine the nature of the signals transmitted between the cortex and the thalamus. By performing, for the first time, high spatiotemporal mesoscopic imaging on tree shrews (the primate's closest relative) through the combination of voltage-sensitive dye recordings and brain stimulation, we revealed clear evidence of distinct thalamocortical functional connectivity pattern originating from the geniculate nucleus and the pulvinar nuclei.
The thalamus is a diencephalic symmetrical ovalshaped mass located between the brainstem below and the telencephalon above, from the posterior commissure to the foramen of Monro. The medial aspect is observable after a sagittal section through the third ventricle. The stria medullaris thalami starting from the ganglion habenulae goes up to the anterior tubercle with the taenia thalami. This is the line of attachment of the tela that forms the roof of the third ventricle. The medial view of the thalamus shows two parts in relation to the line of attachment: below is ventricular or periventricular and above is extraventricular. In many species, there is in the third ventricle an adhaesio interthalamica. This is missing in 30% of the human cases, not depending on gender or age. Furthermore, the chapter discusses which cerebral elements really belong to the thalamus. The tradition relied on large ontogenic, embryologic subdivisions. Recent studies, using gene expression, favor the "neuromeric model." In this model, the hypothalamus is no more diencephalic.
Our evidence from both cytoarchitecture and studies of connections suggests that LE GROS CLARK was correct in postulating that the lateral posterior nucleus of primitive mammals is the homologue to the primate pulvinar. It seems evident that during mammalian evolution both this region of the thalamus and its cortical target have grown larger and more complex. Truly intrinsic subdivisions may have appeared not only in the primates but also independently in other mammalian lines of descent, such as the carnivores. One main goal of our laboratory is to ask how functional subdivisions are related to the increasing subdivisions of structure. Our hope is that this line of inquiry might contribute to an understanding of those functions most recently evolved in mammalian evolution.
The projections of the superior colliculus to the thalamus have been studied in the monkey, Macaca mulatta, with anterograde degeneration techniques. The superior colliculus has been shown to project to the inferior nucleus of the pulvinar in a topographical manner with the lower visual field represented dorsomedially and the upper field ventrolaterally. The peripheral zone is located along the medial border and the fovea at the dorsolateral angle adjacent to the lateral geniculate nucleus. The superior colliculus also sends a dense projection to the ipsilateral intralaminar complex, i.e., to the parafascicular, central lateral and paracentral nuclei, and a lesser projection to the same contralateral nuclei. Degenerating tectal fibers were also found in the lateral geniculate nuclei. Four types of vesicle containing profiles were observed in the inferior pulvinar and paracentral nucleus. The large RL and small RS terminals contain round vesicles of uniform size and form asymmetric contacts mainly with large and small dendrites respectively. The F terminal contains a mixture of small round and flat vesicles. It forms symmetric contacts with dendrites and cell somata. The P profile is very pale and contains a relatively sparse population of vesicles showing a great variation in size. It forms symmetric contacts with medium to large dendrites. It is frequently found postsynaptic to the other types, especially the RL terminal, and is regularly seen as the intermediate element of serial and triadic synaptic arrangements. The experimental electron microscopic study has shown that many fibers from the superior colliculus terminate as RL profiles, undergoing direct dense degeneration, in both the inferior pulvinar and the paracentral nucleus. Others probably end as smaller RS terminals.
Localized microinjections of tritiated amino acids were made in the prestriate cortex (areas 18 and 19) of macaque monkeys in order to determine the topography of the subcortical projections. It was found that the prestriate cortex projected to the entire inferior pulvinar (PI), lateral pulvinar (PL), dorsolateral nucleus, the lateral posterior nucleus, the reticular nucleus, a portion of the medial pulvinar, superior colliculus, and caudate nucleus but not to the dorsal lateral geniculate nucleus. The projections to the PI were organized according to the topographical representation of the contralateral visual hemifield. The ventral portion of the PL which is immediately adjacent to the PI also received a parallel topographical projection in register with the representation of the visual hemifield and thus is distinguished from the remainder of the PL. The dorsal and caudal portions of the PL (which extend to form the lateral portion of the caudal pole of the pulvinar and are located away from PI) also received projections from prestriate cortex which often appeared as several bands of grains. However, although dorsal prestriate cortex seemed to project to the dorsal portion of caudal PL and ventral prestriate cortex seemed to project to the ventral portion of caudal PL, any further topography in the projections to the dorsal and caudal PL as well as any to the other dorsal group nuclei was difficult to determine. The results point to the conclusion that the PI and the immediately adjacent portion of PL are distinguished from the remainder of the pulvinar by their connectional organization, and each region contains a representation of the visual hemifield. Furthermore, the prestriate projections to these and other regions of the pulvinar form the corticothalamic half of visual and visuomotor cortico-thalamocortical projections which involve all the occipital cortices (areas 17, 18 and 19) as well as inferotemporal, parietal and frontal cortices.
An autoradiographic technique was used to determine superior colliculus (SC) and pulvinar projections in the rhesus monkey. SC projects bilaterally to the inferior pulvinar (PI) while occipital cortex projects to PI and the lateral pulvinar (PL). PI has sustaining, topographical projections to layers IV, III and I of areas 18 and 19 (and VI and I of 17) which agrees with the central representation of the visual hemifield and suggests that there is more than one hemifield representation in prestriate cortex. PL adjacent to PI also projects to the same cortical areas and layers, while the portion of PL extending into the caudal pole of the pulvinar projects to layers IV, III and I of areas 20 and 21. Thus, occipital cortices are associated by cortico-thalamocortical connections and also receive direct lemniscal input via SC-PI and the dorsal lateral geniculate nucleus (DLG), while inferotemporal areas 20 and 21 receive only cortico-thalamocortical connections. It is concluded that Stoffels' principle of lamellation holds and, that one pulvinar subdivision projects to several cortical areas, that adjacent pulvinar subdivisions have overlapping projections to these cortical areas and their layers and that the pulvinar also projects to the same cortical area as DLG but to different layers. These connections are similar to those in lower mammals but not to those in the squirrel monkey and bushbaby.
We studied and compared the ipsilateral efferents of the superficial and deep layers of the superior colliculus of the rhesus monkey. Using a stereotaxic method, microelectrodes were inserted through the contralateral hemisphere in order to make electrolytic lesions of the superior colliculus. Large lesions involved all layers of the superior colliculus, while smaller lesions involved either the superficial or the deep layers of the superior colliculus. Following various survival times, the brains were prepared with the Fink-Heimer technique ('67). Following lesions of the superficial layers of the superior colliculus, definite degenerated axonal endings were found in the dorsal and ventral lateral geniculate nuclei, inferior pulvinar, centrointermediate nucleus, magnocellular dorsomedial nucleus, anterior pretectal nucleus and pretectal region. Sparse degenerated axonal endings were found in the limitans nucleus, lateral posterior nucleus and some intralaminar nuclei following lesions of the superficial layers in the rostral portion of the superior colliculus. Following lesions of the deep layers of the superior colliculus, degenerated axonal endings were found in the central gray, magnocellular medial geniculate nucleus, suprageniculate nucleus, limitans nucleus, lateral posterior nucleus, medial and oral pulvinar, nucleus of the accessory optic tract, zona incerta, subdivisions of the ventral lateral and ventral posterior lateral nuclei, ventral posterior inferior nucleus, denosocellular and multiform dorsomedial nuclei, all intralaminar nuclei, inferior colliculus, parabigeminal nucleus, olivary nucleus, reunions nucleus, Forel's Field H and an undefined midbrain nucleus. In general the projections were topographically organized in that the caudal portion of the superior colliculus projected to the rostral portions of thalamic nuclei and the rostral portion of the superior colliculus projected to the caudal portions of thalamic nuclei. All the degeneration patterns seen after lesions of the superficial and deep layers were accounted for by large lesions which involved all layers of the superior colliculus. It is concluded that the superficial and deep layers of the rehesus monkey superior colliculus have different ascending projections. The finding, are related to the organization of visual and multimodal thalamocortical systems in primates and other mammals.
Anatomical material from two series of monkeys (Macaca mulatta) was used to determine the full extent and visuotopic organization of striate projections to the pulvinar. One series was processed for degeneration by the Fink‐Heimer procedure following unilateral lesions of lateral, posterior, or medial striate cortex (representing the central, peripheral, and far peripheral visual field, respectively); collectively, the lesions included all of area 17. The second series was processed for autoradiography following tritiated amino‐acid injections into striate sites representing the center of gaze and eccentricities ranging from 0.5° to greater than 30° from fixation in both the upper and lower fields.
The results indicate the existence of two separate striate projection zones within the pulvinar. One, the PI/PL zone, is located primarily within the inferiorpulvinar (PI) but extends into the adjacentlateral pulvinar (PL). The other, the PL zone, is located entirely within the lateral pulvinar and partially surrounds the first zone along its dorsal, lateral, and ventral aspects.
Within the PI/PL zone, striate projections are topographically organized and represent the entire contralateral visual field. Central vision is represented laterally and posteriorly, with the fovea represented at the caudal pole of the nucleus; conversely, far peripheral vision is found medially and anteriorly, adjacent to the medial geniculate nucleus. The representation of the horizontal meridian runs obliquely across PI/PL, such that the upper visual field is located ventrolaterally and the lower visual field dorsomedially. The representation of the vertical meridian is located along the lateral margin of PI in anterior sections of the pulvinar, but within PL in posterior sections. Thus, the vertical meridian appears to form the border between the lateral margin of the PI/PL zone and the medial margin of the PL zone. At the lateral margin of the PL zone is the representation of its horizontal meridian. Striate projections to the PL zone, unlike those to the PI/PL zone, are limited to the representation of central vision. These results suggest that striate inputs contribute to the visual properties of neurons (Bender, 1981 a) throughout the PI/PL zone, but are insufficient to explain the visual properties of neurons outside of the central visual field representation in the PL zone.
The responses to visual stimuli of neurons in the inferior pulvinar were studied in immobilized monkeys anesthetized with nitrous oxide. Most cells had well-defined receptive fields and responded strongly to stationary or moving spots and slits of light. Receptive fields ranged, on the average, from 1 to 5° in diameter. Although nonvisual stimuli could alter the pattern of spontaneous activity, they did not evoke repeatable, time-locked responses comparable to those evoked by visual stimuli. About a third of the cells were insensitive to stimulus orientation. These cells responded to spots or slits moved through the receptive field in any direction and to stationary slits flashed at any orientation. Two-thirds of the cells were sensitive to the orientation of a moving stimulus. About half of these responded equally well to the two directions of movement of a properly oriented slit; most were also sensitive to the orientation of a stationary flashed slit. The remaining cells were sensitive to the direction of movement: they responded best to stimulus movement in one direction and were inhibited or failed to respond for movement in the opposite direction. A third of these directional cells were also sensitive to the orientation of stationary slits. Most cells showed a pronounced moment-to-moment fluctuation in their visual responsiveness. Responsiveness was often correlated with the level of arousal as reflected in the electroencephalogram (EEG). A number of orientation-sensitive cells exhibited a pronounced afterdischarge, some continuing to discharge for up to 10 s after stimulus offset. The results support the notion that the inferior pulvinar receives visual information from striate cortex. It is suggested that the response of pulvinar cells to this input may be modulated both by the general level of arousal and by visuooculomotor information derived from the superior colliculus.
The retinotopic organization of the inferior and lateral pulvinar in rhesus monkeys was investigated using tungsten microelectrodes and extracellular recordings. The animals were immobilized with gallamine triethiodide and anesthetized with a nitrous oxide-oxygen mixture. Both the inferior and lateral nuclei were found to be visually responsive. Two complete representations of the contralateral hemifield occupy most of this territory. One representation lies mainly within the inferior pulvinar but extends somewhat into the adjacent lateral pulvinar. The vertical meridian lies in the dorsal and lateral margins of the inferior pulvinar while the periphery is found in the medial margin adjacent to the medial geniculate body. The fovea and central vision are represented laterally and posteriorly. A second representation of the hemifield lies entirely within the lateral pulvinar and partially surrounds the first along its dorsal, lateral, ventral, and caudal aspects. The lower quadrant of te second map lies in the dorsal half of the lateral pulvinar, the upper quadrant is found almost completely separated in the ventral half. A double representation of the horizontal meridian forms the outer boundary of the second representation and lies in the external margin of the pulvinar. The two maps share a common representation of the vertical meridian and the pattern of topography reverses in crossing this joint boundary from one map to the other. The physiologically defined boundary between the two representations, i.e., the representation of the vertical meridian, does not coincide with the cytoarchitectonic boundary between the inferior and lateral nuclei but, instead, coincides with the medial edge of a fiber system that fills the external half of the lateral pulvinar. Both visuotopic maps encompass virtually the entire visual hemifield. Receptive-field size for cell clusters in te two visuotopic zones is the same and, for both regions, increases with increasing eccentricity.
The autoradiographic tracing method has been used to analyze the distribution of ascending tectofugal pathways in the rhesus monkey.
Our findings show that axons which arise from deep collicular neurons terminate within several dorsal thalamic nuclei which in turn project upon the frontal eye fields (area 8) and the inferior parietal lobule (area 7). Both of these cortical areas are functionally quite similar to the deep colliculus, and we suggest that ascending channels from the deep tectum must account, at least in part, for these functional similarities.
The present autoradiographs reveal projections to several nuclear zones previously not identified as deep collicular targets in the monkey. Such targets include the visceral cell columns of the oculomotor complex, the rostral interstitial nucleus of the medial longitudinal fasciculus, and the magnocellular division of the ventral anterior nucleus.
Deep tectal input also has been shown to terminate quite extensively within the paralamellar region of the mediodorsal nucleus and in the parafascicular nucleus; very little input to the central lateral and centromedian nuclei was observed.
Radioisotope injections restricted to the superficial layers reveal dense projections to the parabigeminal nucleus, the pretectum, the inferior and lateral pulvinar nuclei, and to the ventral and dorsal lateral geniculate nuclei. Transported protein within the dorsal lateral geniculate nucleus occupied the “S” layers and the interlaminar zones.