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Optical Imaging of Functional Organization in the Monkey Inferotemporal Cortex
Abstract
To investigate the functional organization of object recognition, the technique of optical imaging was applied to the primate
inferotemporal cortex, which is thought to be essential for object recognition. The features critical for the activation of
single cells were first determined in unit recordings with electrodes. In the subsequent optical imaging, presentation of
the critical features activated patchy regions around 0.5 millimeters in diameter, covering the site of the electrode penetration
at which the critical feature had been determined. Because signals in optical imaging reflect average neuronal activities
in the regions, the result directly indicates the regional clustering of cells responding to similar features.
... What is the relationship between perceptograms and the preferred stimuli of their driving neurons? IT cortex is known for its strong object selectivity at the single cell 25,26 as well as~1 mm 3 tissue scale 21,27,28 . While the current OptoArray technology doesn't allow neural recording, rendering us blind with respect to the object selectivity profile of the stimulated neurons, it is reasonable to assume heterogeneity of selectivity at the spatial scale perturbed by a single LED 4,21 in that the perturbed neural population conserves visual preference for a part of the shape space. ...
... IT cortex is known for its strong object selectivity at the single cell 25,26 as well as~1 mm 3 tissue scale 21,27,28 . While the current OptoArray technology doesn't allow neural recording, rendering us blind with respect to the object selectivity profile of the stimulated neurons, it is reasonable to assume heterogeneity of selectivity at the spatial scale perturbed by a single LED 4,21 in that the perturbed neural population conserves visual preference for a part of the shape space. Is perceptography simply another way to measure the stimulus preference of the stimulated neurons? ...
Neurons in the inferotemporal (IT) cortex respond selectively to complex visual features, implying their role in object perception. However, perception is subjective and cannot be read out from neural responses; thus, bridging the causal gap between neural activity and perception demands independent characterization of perception. Historically, though, the complexity of the perceptual alterations induced by artificial stimulation of IT cortex has rendered them impossible to quantify. To address this old problem, we tasked male macaque monkeys to detect and report optical impulses delivered to their IT cortex. Combining machine learning with high-throughput behavioral optogenetics, we generated complex and highly specific images that were hard for the animal to distinguish from the state of being cortically stimulated. These images, named “perceptograms” for the first time, reveal and depict the contents of the complex hallucinatory percepts induced by local neural perturbation in IT cortex. Furthermore, we found that the nature and magnitude of these hallucinations highly depend on concurrent visual input, stimulation location, and intensity. Objective characterization of stimulation-induced perceptual events opens the door to developing a mechanistic theory of visual perception. Further, it enables us to make better visual prosthetic devices and gain a greater understanding of visual hallucinations in mental disorders.
... It is made A feature that is expected to emerge from examination of perceptograms is a common visual element in perceptograms obtained from the same channel. IT cortex is known for its strong object selectivity at the single cell 17,18 as well as ~1mm 3 tissue scale [19][20][21] . While the current OptoArray technology doesn't allow neural recording, rendering us blind with respect to the object selectivity profile of the stimulated neurons, it is reasonable to assume heterogeneity of selectivity at the spatial scale perturbed by a single LED 6,19 in that the perturbed neural population conserves visual selectivity for "a" part of the shape space. ...
... IT cortex is known for its strong object selectivity at the single cell 17,18 as well as ~1mm 3 tissue scale [19][20][21] . While the current OptoArray technology doesn't allow neural recording, rendering us blind with respect to the object selectivity profile of the stimulated neurons, it is reasonable to assume heterogeneity of selectivity at the spatial scale perturbed by a single LED 6,19 in that the perturbed neural population conserves visual selectivity for "a" part of the shape space. Assuming this, one might Fig S1). ...
Neurons in the inferotemporal (IT) cortex respond selectively to complex visual features, implying their role in object perception. However, perception is subjective and cannot be read out from neural responses; thus, bridging the causal gap between neural activity and perception demands independent characterization of perception. Historically though, the complexity of the perceptual alterations induced by artificial stimulation of IT cortex has rendered them impossible to quantify. Here we addressed this old problem by combining machine learning with high-throughput behavioral optogenetics in macaque monkeys. In closed-loop experiments, we generated complex and highly specific images that the animal could not discriminate from the state of being cortically stimulated. These images, named “perceptograms” for the first time, reveal and depict the contents of the complex hallucinatory percepts induced by local neural perturbation in IT cortex. Furthermore, we found that the nature and magnitude of these hallucinations highly depend on concurrent visual input, stimulation location, and intensity. Objective characterization of stimulation-induced perceptual events opens the door to developing a mechanistic theory of visual perception. Further, it enables us to make better visual prosthetic devices and gain a greater understanding of visual hallucinations in mental disorders.
One-Sentence Summary
Combining state-of-the-art AI with high-throughput closed-loop brain stimulation experiments, for the first time, we took “pictures” of the complex and subjective visual hallucinations induced by local stimulation in the inferior temporal cortex, a cortical area associated with object recognition.
... In the 1980s, electrophysiological studies involving NHPs identified visually responsive neurons in the IT cortex that were selective for various categories, including faces Bruce et al., 1981;Desimone et al., 1984;Perrett et al., 1982). A subsequent optical imaging study revealed clusters of face-selective cells within a small region of the IT cortex (Wang et al., 1996). Further fMRI studies scanned the whole brain and found multiple face-selective areas distributed across the IT cortices of primates, including those of humans (Kanwisher et al., 1997), macaques (Logothetis et al., 1999;Tsao et al., 2003), and marmosets (Dureux et al., 2023;Hung et al., 2015). ...
Humans and primates rely on visual face recognition for social interactions. Damage to specific brain areas causes prosopagnosia, a condition characterized by the inability to recognize familiar faces, indicating the presence of specialized brain areas for facial‐recognition processing. A breakthrough finding came from a non‐human primate (NHP) study conducted in the early 2000s; it was the first to identify multiple face‐processing areas in the temporal lobe, termed “face patches.” Subsequent studies have demonstrated the unique role of each face patch in the structural analysis of faces. More recent studies have expanded these findings by exploring the role of face‐patch networks in social and memory functions and the importance of early face exposure in the development of the system. In this review, we discuss the neuronal mechanisms responsible for analyzing facial features, categorizing faces, and associating faces with memory and social contexts within both the cerebral cortex and subcortical areas. Use of NHPs in neuropsychological and neurophysiological studies can highlight the mechanistic aspects of the neuronal circuit underlying face recognition at both the single‐neuron and whole‐brain network levels.
... [25][26][27] In the ITC and the PFC, electrophysiological and imaging studies have revealed functional organization for representing faces, colors, and various visual features. [28][29][30][31][32] Furthermore, a study using electrocorticography (ECoG) and pattern classification analysis has shown that theta-band neural oscillations are organized in the ITC, particularly concerning memory retrieval. 33 It is hypothesized, based on these findings, that information flows via neural oscillations between the ITC and the PFC related to memory retrieval and WM maintenance processes are also organized in these regions, but this has not yet been established. ...
Interaction between the inferotemporal (ITC) and prefrontal (PFC) cortices is critical for retrieving information from memory and maintaining it in working memory. Neural oscillations provide a mechanism for communication between brain regions. However, it remains unknown how information flow via neural oscillations is functionally organized in these cortices during these processes. In this study, we apply Granger causality analysis to electrocorticographic signals from both cortices of monkeys performing visual association tasks to map information flow. Our results reveal regions within the ITC where information flow to and from the PFC increases via specific frequency oscillations to form clusters during memory retrieval and maintenance. Theta-band information flow in both directions increases in similar regions in both cortices, suggesting reciprocal information exchange in those regions. These findings suggest that specific subregions function as nodes in the memory information-processing network between the ITC and the PFC.
... Yet it is hard not to speculate about the neural underpinnings of the observed effects. Stimulation of ~1 cubic millimeter of tissue by activation of 1 LED on the array (Rajalingham et al. 2021) is expected to engage IT cortex at a scale that still preserves object category selectivity (Wang, Tanaka, and Tanifuji 1996;Tsao et al. 2006;Lafer-Sousa and Conway 2013;Sato et al. 2013). The fact that behavioral detection of local cortical perturbation of this scale interacts differentially with various objects is consistent with the heterogeneity of object responses across IT cortex. ...
To be able to effectively restore vision by direct cortical stimulation, we need to understand the perceptual events induced by stimulation of high-level visual cortices. We trained macaque monkeys to detect and report optogenetic impulses delivered to their inferior temporal cortices. In a series of experiments, we observed that detection of cortical stimulation is highly dependent on the choice of images presented to the eyes and that detection of cortical stimulation is most difficult when the animal fixates on a blank screen. We show that optogenetic stimulation of object-selective parts of the visual cortex induces perceptual events that are easy to detect, probably as object-dependent distortions of the concurrent contents of vision. These findings invite expanding the scope of visual prosthetics beyond the primary visual cortex.
... Yet it is hard not to speculate about the neural underpinnings of the observed effects. Stimulation of ~1 cubic millimeter of tissue by activation of 1 LED on the array (Rajalingham et al. 2021) is expected to engage IT cortex at a scale that still preserves object category selectivity (Wang, Tanaka, and Tanifuji 1996;Tsao et al. 2006;Lafer-Sousa and Conway 2013;Sato et al. 2013). The fact that behavioral detection of local cortical perturbation of this scale interacts differentially with various objects is consistent with the heterogeneity of object responses across IT cortex. ...
To be able to effectively restore vision by direct cortical stimulation, we need to understand the perceptual events induced by stimulation of high-level visual cortices. We trained macaque monkeys to detect and report optogenetic impulses delivered to their inferior temporal cortices. In a series of experiments, we observed that detection of cortical stimulation highly depends on the choice of images presented to the eyes and that detection of cortical stimulation is most difficult when the animal fixates on a blank screen. We show that local stimulation of object selective parts of the visual cortex induce perceptual events that are easy to detect as object-dependent distortions of the concurrent contents of vision. These findings invite expanding the scope of visual prosthetics beyond the primary visual cortex.
Értekezésemben a főemlős agykéreg pályajelöléssel feltérképezett anatómiaia hálózatának elméleten és kísérleten alapuló kutatásával kapcsolatos eredményeimet foglalom össze. Célom volt a nagy léptékű integráció, a populációk összeköttetési mintázatainak és az elemi építőegységek, az axonok és axonvégződések szerepének megértése a hálózat szerveződésében. Kimutattam, hogy a kompartmentalizált hálózatban az elsődleges érzőkérgi áreák szintjén a heteromodális integráció a magasabb hierarchia szintek multimodális struktúráinak híd szerepével magyarázható. A konvergenciafok bevezetésével a csúcsok és élek tulajdonságain keresztül meghatároztam az agykérgi jelfolyam egyedi jellemzőit. Így a prefrontális kéregben (PFC) kimutattam az áreák topológián alapuló hierarchiáját. Szintén kimutattam, hogy egyes PFC-áreák globális konvergencia régiók, emiatt hálózati szűk keresztmetszetként limitálhatják a munkamemória kapacitását. Rámutattam, hogy a PFC funkciója a magas szintű áreákkal interakcióban valósul meg a „globális munkatérben”. A kolumnák hálózatában área 3b és 1 oldalirányú összeköttetésein bizonyítottam, hogy az interakciók áreán belül az eltérő, áreák között elsődlegesen a hasonló funkciót reprezentáló populációk között alakulnak ki. Ugyanitt meghatároztam a köztes szintű hálózati motívumot és szerepét a populációs válaszban. Kimutattam a kérgi hálózat éleinek heterogén struktúráját és szerepét az összeköttetésekben mind a vezetőképességet befolyásoló axonmorfológiában és a szinaptikus boutonok jelátvitel hatékonyságát jellemző morfológiájában. Bizonyítékot szolgáltattam a nem-szövetspecifikus alkalikus foszfatáz (TNAP) réteg-specifikus lokalizációjára a szinaptikus résben. Feltártam, hogy a molekuláris hálózatban a TNAP többféle módon képes szabályozni a jelátvitelt.
Recognizing faces regardless of their viewpoint is critical for social interactions. Traditional theories hold that view-selective early visual representations gradually become tolerant to viewpoint changes along the ventral visual hierarchy. Newer theories, based on single-neuron monkey electrophysiological recordings, suggest a three-stage architecture including an intermediate face-selective patch abruptly achieving invariance to mirror-symmetric face views. Human studies combining neuroimaging and multivariate pattern analysis (MVPA) have provided convergent evidence of view selectivity in early visual areas. However, contradictory conclusions have been reached concerning the existence in humans of a mirror-symmetric representation like that observed in macaques. We believe these contradictions arise from low-level stimulus confounds and data analysis choices. To probe for low-level confounds, we analyzed images from two face databases. Analyses of image luminance and contrast revealed biases across face views described by even polynomials-i.e., mirror-symmetric. To explain major trends across neuroimaging studies, we constructed a network model incorporating three constraints: cortical magnification, convergent feedforward projections, and interhemispheric connections. Given the identified low-level biases, we show that a gradual increase of interhemispheric connections across network-layers is sufficient to replicate view-tuning in early processing stages and mirror-symmetry in later stages. Data analysis decisions-pattern dissimilarity measure and data recentering-accounted for the inconsistent observation of mirror-symmetry across prior studies. Pattern analyses of human fMRI data (of either sex) revealed biases compatible with our model. The model provides a unifying explanation of MVPA studies of viewpoint selectivity and suggests observations of mirror-symmetry originate from ineffectively normalized signal imbalances across different face views.
Artificial activation of neurons in early visual areas induces perception of simple visual flashes.¹,² Accordingly, stimulation in high-level visual cortices is expected to induce perception of complex features.³,⁴ However, results from studies in human patients challenge this expectation. Stimulation rarely induces any detectable visual event, and never a complex one, in human subjects with closed eyes.² Stimulation of the face-selective cortex in a human patient led to remarkable hallucinations only while the subject was looking at faces.⁵ In contrast, stimulations of color- and face-selective sites evoke notable hallucinations independent of the object being viewed.⁶ These anecdotal observations suggest that stimulation of high-level visual cortex can evoke perception of complex visual features, but these effects depend on the availability and content of visual input. In this study, we introduce a novel psychophysical task to systematically investigate characteristics of the perceptual events evoked by optogenetic stimulation of macaque inferior temporal (IT) cortex. We trained macaque monkeys to detect and report optogenetic impulses delivered to their IT cortices⁷,⁸,⁹ while holding fixation on object images. In a series of experiments, we show that detection of cortical stimulation is highly dependent on the choice of images presented to the eyes and it is most difficult when fixating on a blank screen. These findings suggest that optogenetic stimulation of high-level visual cortex results in easily detectable distortions of the concurrent contents of vision.
To understand the underlying neuronal representation for object recognition, we designed this study to investigate the changes in N1, the first negative event-related potential component, accompanied by object discrimination learning. Subjects were asked to train themselves to recognize novel computer-made objects by performing an object discrimination task, in which an object had to be discriminated from others regardless of the change in viewing angle. Such object discrimination did not cause any significant change in either the averaged N1 amplitude or the averaged amplitude delay over the subjects. However, the dipole source analysis for N1 found statistically significant displacement of estimated dipole location caused by object discrimination training in the right hemisphere. The source obtained after training located significantly laterally than that obtained before training. The finding demonstrates the difference in neuronal representations of the experienced objects before and after view-invariant object discrimination learning, and suggests the different neuronal representations for object recognition with novel objects and familiar objects.
Previous studies have reported that some neurons in the inferior temporal (IT) cortex respond selectively to highly specific complex objects. In the present study, we conducted the first systematic survey of the responses of IT neurons to both simple stimuli, such as edges and bars, and highly complex stimuli, such as models of flowers, snakes, hands, and faces. If a neuron responded to any of these stimuli, we attempted to isolate the critical stimulus features underlying the response. We found that many of the responsive neurons responded well to virtually every stimulus tested. The remaining, stimulus-selective cells were often selective along the dimensions of shape, color, or texture of a stimulus, and this selectivity was maintained throughout a large receptive field. Although most IT neurons do not appear to be "detectors" for complex objects, we did find a separate population of cells that responded selectively to faces. The responses of these cells were dependent on the configuration of specific face features, and their selectivity was maintained over changes in stimulus size and position. A particularly high incidence of such cells was found deep in the superior temporal sulcus. These results indicate that there may be specialized mechanisms for the analysis of faces in IT cortex.
Maps of orientation preference and selectivity, inferred from differential images of orientation (Blasdel, 1992), reveal linear organizations in patches, 0.5-1.0 mm across, where orientation selectivities are high, and where preferred orientations rotate linearly along one axis while remaining constant along the other. Most of these linear zones lie between the centers of adjacent ocular dominance columns, with their short iso-orientation slabs oriented perpendicular, in regions enjoying the greatest binocular overlap. These two-dimensional linear zones are segregated by one- and zero-dimensional discontinuities that are particularly abundant in the centers of ocular dominance columns, and that are also correlated with cytochrome oxidase-rich zones within them. Discontinuities smaller than 90 degrees extend in one dimension, as fractures, while discontinuities greater than 90 degrees are confined to points, in the form of singularities, that are generated when orientation preferences rotate continuously through +/- 180 degrees along circular paths. The continuous rotations through 180 degrees imply that direction preferences are not organized laterally in striate cortex. And they also ensure that preferences for all orientations converge at each singularity, with perpendicular orientations represented uniquely close together on opposite sides. The periodic interspersing of linear zones and singularities suggests that orientation preferences are organized by at least two competing schemes. They are optimized for linearity, along with selectivity and binocularity, in the linear zones, and they are optimized for density near singularities. Since upper-layer neurons are likely to have similarly sized dendritic fields in all regions (Lund and Yoshioka, 1991), those in the linear zones should receive precise information about narrowly constrained orientations, while those near singularities should receive coarse information about all orientations--very different inputs that suggest different perceptual functions.
At early stages of the mammalian visual cortex, neurons with similar stimulus selectivities are vertically arrayed through the thickness of the cortical sheet and clustered in patches or bands across the surface. This organization, referred to as a 'column', has been found with respect to one-dimensional stimulus parameters such as orientation of stimulus contours, eye dominance of visual inputs, and direction of stimulus motion. It is unclear, however, whether information with extremely high dimensions, such as visual shape, is organized in a similar columnar fashion or in a different manner in the brain. Here we report that the anterior inferotemporal area of the monkey cortex, the final station of the visual cortical stream crucial for object recognition, consists of columns, each containing cells responsive to similar visual features of objects.
Differential images of ocular dominance, acquired by comparing responses to the two eyes, reveal dark and light bands where cortical cells are dominated by the right and left eyes. These include most (but not all) histochemically stained cytochrome oxidase blobs in their centers. Differential images of orientation, acquired by comparing responses to orthogonal orientations, reveal dark and light bands that are reminiscent of the "orientation columns" reported earlier, on the basis of 2-deoxyglucose (2DG) autoradiograms (Hubel et al., 1978). However, they are shorter and more fragmented because they do not include regions lacking selectivity for orientation. Even though these "bands" derive from orientation-selective areas, comparisons with differential images of other orientations reveal that regions along their centers prefer different orientations. Hence, the orientation preferences inferred from "bands" in single differential images, or single 2DG autoradiograms, are not necessarily incorrect. Interactions between ocular dominance and orientation were investigated by comparing differential images of orientation obtained with binocular and monocular stimulation, as well as by comparing differential images of ocular dominance obtained with different orientations. In both cases, the elicited interactions were minimal, indicating a remarkable and unexpected independence that subsequent experiments revealed arises, at least in part, from a lateral segregation of regions most selective for one eye and regions most selective for one orientation, in the centers and edges of ocular dominance columns. Since this can also be viewed as a lateral correlation between binocularity and orientation selectivity, it fits with the simultaneous emergence of these properties in layers receiving input from layer 4c, and suggests that each of these properties requires the other.
The responses of somatosensory cortex (S-I) to tactile stimulation of the forepaw were assessed by intrinsic signal optical imaging. The tips of digits two or five were alternately touched with mechanical tappers while video photographs were taken of S-I illuminated by an 800-nm light source. The resulting images showed two highlighted areas about 300 microns in diameter and 500 microns apart. Generation of these images required less than 1 hr. Electrode penetrations placed in the areas highlighted during stimulation provided multiunit recordings with receptive fields appropriate for the stimulated digit and not the other digit. Penetrations between the high-lighted areas yielded receptive fields on intervening digits. These results demonstrate that intrinsic signal optical images are obtainable in S-I and confirm the functional somatotopy previously reported using electrical recording. Furthermore, the short time required to produce the images and the obtainable spatial resolution suggest that optical recording could be employed for the study of cortical reorganization in this brain region.
Optical imaging of the functional architecture of cortex, based on intrinsic signals, is a useful tool for the study of the development, organization, and function of the living mammalian brain. This relatively noninvasive technique is based on small activity-dependent changes of the optical properties of cortex. Thus far, functional imaging has been performed only on anesthetized animals. Here we establish that this technique is also suitable for exploring the brain of awake behaving primates. We designed a chronic sealed chamber and mounted it on the skull of a cynomolgus monkey (Macaca fascicularis) over the primary visual cortex to permit imaging through a transparent glass window. Restriction of head position alone was sufficient to eliminate movement noise in awake monkey imaging experiments. High-resolution imaging of the ocular dominance columns and the cytochrome oxidase blobs was achieved simply by taking pictures of the exposed cortex when the awake monkey was viewing video movies alternatively with each eye. Furthermore, the functional maps could be obtained without synchronization of the data acquisition to the animal's respiration and the electrocardiogram. The wavelength dependency and time course of the intrinsic signal were similar in anesthetized and awake monkeys, indicating that the signal sources were the same. We therefore conclude that optical imaging is well suited for exploring functional organization related to higher cognitive brain functions of the primate as well as providing a diagnostic tool for delineating functional cortical borders and assessing proper functions of human patients during neurosurgery.
Imaging analysis techniques were used to examine changes in the intrinsic optical properties in hippocampal brain slices that occurred during synaptic activity evoked by Schaffer collateral stimulation in CA1. Repetitive synaptic activity was associated with an increase in light transmission in the synaptic region in stratum radiatum. The effect was seen at wavelengths of light between 450 and 800 nm but was of greater amplitude at longer wavelengths. Blocking synaptic transmission with either Ca(2+)-free EGTA perfusate or kynurenic acid (an excitatory amino acid antagonist) blocked the optical signal, indicating that it resulted from postsynaptic activation of the cells and was not due to presynaptic fiber volleys or transmitter release alone. Because the optical changes were blocked by reducing extracellular Cl- (by replacement with gluconate) or by furosemide (an anion transport inhibitor), increased Cl- transport (conceivably Na-K-2Cl cotransport) may generate these signals possibly by causing cellular swelling and thereby less light scattering. These optical changes were not blocked, however, by bicarbonate-free solution, indicating that bicarbonate transport may not be involved. Changes in the intrinsic optical signal could be related to glial swelling due to K+ released during neuronal activity because high-K(+)-induced swelling of cultured astrocytes is blocked by furosemide and low-Cl- solution. Intrinsic optical signals of neuronal tissue should be considered when voltage- or ion-sensitive dyes are used.
Functional interactions among inferior temporal cortex (IT) neurons were studied in the awake, fixating macaque monkey during the presentation of visual stimuli. Extracellular recordings were obtained simultaneously from several microelectrodes, and in many cases, spike trains from more than one neuron were extracted from each electrode by the use of spike shape sorting technology. Functional interactions between pairs of neurons were measured using cross-correlation. Discharge patterns of single neurons were evaluated using auto-correlation and PST histograms. Neurons recorded on the same electrode (within about 100 microns) had more similar stimulus selectivity and were more likely to show functional interactions than those recorded on different electrodes spaced about 250 to 500 microns apart. Most neurons tended to fire in bursts tens to hundreds of milliseconds in duration, and asynchronously from the stimulus induced rate changes. Correlated neuronal firing indicative of shared inputs and direct interactions was observed. Occurrence of shared input was significantly lower for neuron pairs recorded on different electrodes than for neurons recorded on the same electrode. Direct connections occurred about as often for neurons on different electrodes as for neurons on the same electrode. These results suggest that input projections are usually restricted to less than 500 micron patches and are then distributed over greater distances by intrinsic connections. Measurements of synaptic contribution suggest that typically more than 5 near-simultaneous inputs are required to cause an IT neuron to discharge.
The mammalian cortex is organized in a columnar fashion: neurons lying below each other from the pia to the white matter usually share many functional properties. Across the cortical surface, cells with similar response properties are also clustered together, forming elongated bands or patches. Some response properties, such as orientation preference in the visual cortex, change gradually across the cortical surface forming 'orientation maps'. To determine the precise layout of iso-orientation domains, knowledge of responses not only to one but to many stimulus orientations is essential. Therefore, the exact depiction of orientation maps has been hampered by technical difficulties and remained controversial for almost thirty years. Here we use in vivo optical imaging based on intrinsic signals to gather information on the responses of a piece of cortex to gratings in many different orientations. This complete set of responses then provides detailed information on the structure of the orientation map in a large patch of cortex from area 18 of the cat. We find that cortical regions that respond best to one orientation form highly ordered patches rather than elongated bands. These iso-orientation patches are organized around 'orientation centres', producing pinwheel-like patterns in which the orientation preference of cells is changing continuously across the cortex. We have also analysed our data for fast changes in orientation preference and find that these 'fractures' are limited to the orientation centres. The pinwheels and orientation centres are such a prominent organizational feature that it should be important to understand their development as well as their function in the processing of visual information.
Optical imaging of animal somatosensory, olfactory and visual cortices has revealed maps of functional activity. In non-human primates, high-resolution maps of the visual cortex have been obtained using only an intrinsic reflection signal. Although the time course of the signal is slower than membrane potential changes, the maximum optical changes correspond to the maximal neuronal activity. The intrinsic optical signal may represent the flow of ionic currents, oxygen delivery, changes in blood volume, potassium accumulation or glial swelling. Here we use similar techniques to obtain maps from human cortex during stimulation-evoked epileptiform afterdischarges and cognitively evoked functional activity. Optical changes increased in magnitude as the intensity and duration of the afterdischarges increased. In areas surrounding the afterdischarge activity, optical changes were in the opposite direction and possibly represent an inhibitory surround. Large optical changes were found in the sensory cortex during tongue movement and in Broca's and Wernicke's language areas during naming exercises. The adaptation of high-resolution optical imaging for use on human cortex provides a new technique for investigation of the organization of the sensory and motor cortices, language, and other cognitive processes.