The contribution of vertical and horizontal connections to the receptive field center and surround in V1.

Here we review the results of anatomical and physiological studies in tree shrew visual cortex which focus on the contribution of vertical and horizontal inputs to receptive field center and surround properties of layer 2/3 neurons. A fundamental feature of both sets of connections is the arrangement of axon arbors in a fashion that respects both the orientation preference and retinotopic displacement of the target site. As a result, layer 2/3 neurons receive convergent input from populations of layer 4 and other layer 2/3 neurons whose receptive fields are displaced along an axis in visual space that corresponds to their preferred orientation. Although, horizontal connections extend for greater distances across the cortical surface than vertical connections, the majority of these inputs link neurons with overlapping receptive fields, emphasizing that both feed-forward and recurrent circuits are likely to play a constructive role in generating properties (such as orientation selectivity) that define the receptive field center. Both within and beyond the dimensions of the receptive field center, the distribution of horizontal connections accords remarkably well with the magnitude and axial tuning of length summation effects. Taken together, these results suggest a continuum of functional properties that transcends the traditional designation of receptive field center and surround. By extension, we suggest that the perceptual effects of stimulus context may arise from stimulus interactions within the receptive field center as well as between center and surround.     

Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex

Neurons in the primary visual cortex of higher mammals are arranged in columns, and the neurons in each column respond best to light-dark borders of particular orientations. The basis of cortical cell orientation selectivity is not known. One possible mechanism would be for cortical cells to receive input from several lateral geniculate nucleus (LGN) neurons with receptive fields that are aligned in the visual field (Hubel and Wiesel, 1962). We have investigated the relationship between the arrangement of the receptive fields of geniculocortical afferents and the orientation preferences of cortical cells in the orientation columns to which the afferents provide visual input. Radial microelectrode penetrations were made into primary visual cortex of anesthetized adult sable ferrets. Cortical cells were recorded throughout the depth of the cortex, and their orientation preferences were determined. Cortical cell responses were then eliminated by superfusion of the cortex with either kainic acid (Zahs and Stryker, 1988) or muscimol. After the drug treatment, responses from many single units with distinct receptive fields were recorded. These responses were presumed to be those of geniculocortical afferents, because they had the response properties characteristic of LGN neurons, and because they could be recorded only in cortical layers that receive geniculate input. In 16 of 18 cases, the afferent receptive fields recorded in a single penetration covered an elongated region of visual space. In these penetrations, the best-fit line through the centers of the afferent receptive fields generally paralleled the preferred orientation of cortical cells recorded at the same site in cortex. These results are consistent with the Hubel and Wiesel (1962) model for the construction of oriented visual cortical receptive fields from geniculate inputs with aligned receptive fields.     

The rabbit and the cat: a comparison of some features of response properties of single cells in the primary visual cortex.

Receptive field characteristics of single cells in primary visual cortex of rabbit were studied. Seventy-two percent of cells were found to be orientation selective, and the remainder had concentric, uniform, movement selective or pure direction selective receptive fields. Single cells were also recorded from primary visual cortex of cat to permit a comparison of visual cortical organization in cats and rabbits. Laminar organization of receptive field types was observed in rabbits which was similar in most respects to that described in the cat. Although the major categories of orientation selective cells (simple, complex, hypercomplex) were similar for both cat and rabbit, many differences emerged: (I) tuning of orientation selectivity was narrower in cats than in rabbits; (II) units which preferred oblique orientations were less frequently represented in rabbits than in cats; (III) orientation preferences appeared to be arranged in clusters in rabbit cortex; in rabbits we found no evidence of the columnar organization of orientation selectivity which characterizes cat visual cortex. A comparison of our data with those previously reported for mouse, rat, hamster and opossum visual cortex suggest that mammals in which a significant proportion of visual cortical cells are not orientation selective have in common certain patterns of cortical organization involving a less precise and less specilized representation of stimulus orientation.     

The retinotopic organization of area 17 (striate cortex) in the cat.

The location and retinotopic organization of visual areas in the cat cortex were determined by systematically mapping visual cortex in over 100 cats. The positions of the receptive fields of single neurons or small clusters of neurons were related to the locations of the corresponding recording sites in the cortex to determine the representations of the visual field in these cortical areas. In this report, the first of a series, we describe the organization of area 17. A single representation of the cat's entire visual field corresponds closely to the cytoarchitectonically defined area 17. This area has the largest cortical surface area (380 mm2) and the highest cortical magnification factor (3.6 mm2/degree2 at area centralis) of all the cortical areas we have studied. There was perfect agreement between the borders of area 17 determined electrophysiologically and cytoarchitecturally. This area contains a first order transformation of the visual hemifield in which every adjacent point in the visual field is represented as an adjacent point in the cortex. Some variability exists among cats in the extent and retinotopic representation of the visual field in area 17.     

Intracellular analysis of directional sensitivity of tectal neurons of the frog

The directional sensitivity of tectal neurons of the frog was examined by means of in vivo whole cell recording technique. Three kinds of stimulus were applied; (1) diffuse light 'on-off', (2) moving dark spot and (3) light spot given at one dimensional grid points. The first stimulus revealed whether or not retinal 'on-off' (R3) or 'off' (R4) fibers contribute to the response. As reported earlier, the following patterns were found for both light 'on' and light 'off': EPSPs only, IPSPs only or a combination of EPSPs and IPSPs. Four directionally sensitive neurons and three non-directionally sensitive neurons were found using the second stimulus. Using the third stimulus, responses at up to 11 positions separated by 2 degrees or 4 degrees were recorded. By measuring the amplitudes of 'on' and 'off' responses at different times, spatio-temporal receptive fields were composed. Two types of directional sensitivity were found. The response of the first type was composed of exclusively excitatory potentials, but the second type was composed of a combination of excitatory and inhibitory potentials. The spatio-temporal receptive field of the second type showed spatially separated excitatory and inhibitory regions with constant latencies. Such simple spatio-temporal receptive field organization was not found for directional sensitive neurons of the cat visual cortex. The spatio-temporal receptive field organization of the second type of directionally sensitive neuron in the present study is in agreement with striated receptive field found in some of the T5 neurons classified by extracellular unit recording [Frog Neurobiology (1976) 297].     

Circuits that build visual cortical receptive fields

Neural sensitivity to basic elements of the visual scene changes dramatically as information is handed from the thalamus to the primary visual cortex in cats. Famously, thalamic neurons are insensitive to stimulus orientation whereas their cortical targets easily resolve small changes in stimulus angle. There are two main types of cells in the visual cortex, simple and complex, defined by the structure of their receptive fields. Simple cells are thought to lay the groundwork for orientation selectivity. This review focuses on approaches that combine anatomy with physiology at the intracellular level, to explore the circuits that build simple receptive fields and that help to maintain neural sensitivity to stimulus features even when luminance contrast changes.     

Model-based analysis of excitatory lateral connections in the visual cortex

Excitatory lateral connections within the primary visual cortex are thought to link neurons with similar receptive field properties. Here we studied whether this rule can predict the distribution of excitatory connections in relation to cortical location and orientation preference in the cat visual cortex. To this end, we obtained orientation maps of areas 17 or 18 using optical imaging and injected anatomical tracers into these regions. The distribution of labeled axonal boutons originating from large populations of excitatory neurons was then analyzed and compared with that of individual pyramidal or spiny stellate cells. We demonstrate that the connection patterns of populations of nearby neurons can be reasonably predicted by Gaussian and von Mises distributions as a function of cortical location and orientation, respectively. The connections were best described by superposition of two components: a spatially extended, orientation-specific and a local, orientation-invariant component. We then fitted the same model to the connections of single cells. The composite pattern of nine excitatory neurons (obtained from seven different animals) was consistent with the assumptions of the model. However, model fits to single cell axonal connections were often poorer and their estimated spatial and orientation tuning functions were highly variable. We conclude that the intrinsic excitatory network is biased to similar cortical locations and orientations but it is composed of neurons showing significant deviations from the population connectivity rule.     

Squirrel visual cortex neurons selective for contour orientation

The receptive field organization of orientation-selective neurons was studied in the squirrel visual cortex. Neurons with mutual inhibiting on- and off-areas of the receptive field, partially and completely overlapping excitatory and inhibitory mechanisms were observed. Neurons of the second group are the most typical. They reveal orientation selectivity if the stimuli are in the excitatory area of the receptive field, the inhibitory areas outside the excitatory area sharpen the selectivity. It is supposed that no obvious differentiation between simple and complex neurons exist in the squirrel visual cortex.     

Functional properties of the corticotectal projection in the golden hamster

Approximately 31% of the cells recorded in the hamster's superior colliculus could be activated by stimulation of the ipsilateral primary visual cortex. While cortically activated cells were encountered in all laminae of the colliculus where visual cells were isolated, the highest probability of driving visual cells was observed in the deeper laminae, that is, those ventral to the stratum opticum. Response latency, jitter (latency variability), latency shifts as a function of shock intensity, thresholds, and spike numbers did not vary as a function of depth in the colliculus. There was a clear correspondence between the visual fields of the best cortical stimulus points and the receptive fields of cortically activated cells recorded in the superficial laminae of the colliculus. However, there was considerably less retinotopic fidelity for the cortical areas from which cells isolated in the deeper laminae could be driven. This suggests a greater degree of convergence from relatively widespread cortical regions upon visual cells of the deeper laminae. The visual response properties (directional selectivity, speed preferences, and receptive field organization) of the cortically activated cells did not differ appreciably from the overall sample of visual cells recorded in the colliculus. Only 3 of the 159 cells tested were driven by stimulation of the contralateral visual cortex and two of these were responsive only at very long latencies.     

Responses of neurons in the Clare-Bishop cortical association area of the cat cerebral cortex to photic stimulation

In acute experiments on cats with protrigeminal section immobilized by flaxedil the electrical activity of single neurons in associative visual cortex of Clare-Bishop was investigated by the extracellular registration of their spike activity. 95.5% of investigated neurons responding to natural stimulation (light spots) were sensitive to the movement of stimulus through the receptive field. Nearly 55% of neurons exhibited selective responses to the direction of stimulus movement. Some neurones responded only when the stimulus was crossing the border points of receptive field. Nearly 85.3% of neurons responded to the flashing spot with "on", "on-off" and "off" reactions, and also to the stimulation by diffuse flashes. Receptive fields of neurons in the Clare-Bishop area were of strip-like form with longitudinal axis in horizontal orientation. Presented observations allow concluding that the Clare-Bishop cortical association area plays an essential role in the central processing of visual information.     

Small-field neurons associated with oculomotor and optomotor control in muscoid flies: functional organization.

In fleshflies, Sarcophaga bullata, intracellular recording and Lucifer yellow dye-filling have revealed small-field elements of sexually isomorphic retinotopic arrays in the lobula and lobula plate, the axons of which project to premotor channels in the deutocerebrum that supply head-turning and flight-steering motor neurons. The dendrites of the small-field elements visit very restricted oval areas of the retinotopic mosaic, comprising fields that are typically 6-8 input columns wide and 12-20 high. Their physiologically determined receptive fields are also small, typically 20 degrees or less in diameter. The neurons are hyperpolarized in stationary illumination and are transiently depolarized by light OFF and to a lesser degree by light ON. Motion of a striped grating elicits a periodic excitation at the fundamental or second harmonic of the stimulus temporal contrast frequency. The arrangement of these elements in retinotopic arrays with their small receptive fields and flicker-sensitive dynamic properties make these neurons well suited for the position-dependent, direction-insensitive detection of small objects in the fly's visual field, which is known to drive fixation and tracking.     

Visual orientation and directional selectivity through thalamic synchrony

Thalamic neurons respond to visual scenes by generating synchronous spike trains on the timescale of 10-20 ms that are very effective at driving cortical targets. Here we demonstrate that this synchronous activity contains unexpectedly rich information about fundamental properties of visual stimuli. We report that the occurrence of synchronous firing of cat thalamic cells with highly overlapping receptive fields is strongly sensitive to the orientation and the direction of motion of the visual stimulus. We show that this stimulus selectivity is robust, remaining relatively unchanged under different contrasts and temporal frequencies (stimulus velocities). A computational analysis based on an integrate-and-fire model of the direct thalamic input to a layer 4 cortical cell reveals a strong correlation between the degree of thalamic synchrony and the nonlinear relationship between cortical membrane potential and the resultant firing rate. Together, these findings suggest a novel population code in the synchronous firing of neurons in the early visual pathway that could serve as the substrate for establishing cortical representations of the visual scene.     

Direction selectivity of excitatory and inhibitory neurons in ferret visual cortex.

Direction selectivity is a characteristic feature of neurons in the visual cortex of higher mammals. Excitatory and inhibitory cortical neurons receive different patterns of synaptic connections resulting in different receptive field properties. We have analyzed the direction tuning of excitatory and inhibitory neurons of ferret visual cortex using single unit recordings. Direction tuning was constant among neurons in a vertical column. The majority (> 80%) of excitatory (regular spiking) neurons were direction tuned or direction biased. Fast spiking (inhibitory) neurons were orientation, but only weakly or not direction tuned. This indicates that excitatory and inhibitory neurons have different functions in visual processing and their different integration in thalamocortical and intracortical circuits results in a diversification of receptive field properties.     

Balanced Enhancements of Synaptic Excitation and Inhibition Underlie Developmental Maturation of Receptive Fields in the Mouse Visual Cortex

Neurons in the developing visual cortex undergo progressive functional maturation as indicated by the refinement of their visual feature selectivity. However, changes of the synaptic architecture underlying the maturation of spatial visual receptive fields (RFs) per se remain largely unclear. Here, loose-patch as well as single-unit recordings in layer 4 of mouse primary visual cortex (V1) of both sexes revealed that RF development following an eye-opening period is marked by an increased proportion of cortical neurons with spatially defined RFs, together with the increased signal-to-noise ratio of spiking responses. By exploring excitatory and inhibitory synaptic RFs with whole-cell voltage-clamp recordings, we observed a balanced enhancement of both synaptic excitation and inhibition, and while the excitatory subfield size remains relatively constant during development, the inhibitory subfield is broadened. This balanced developmental strengthening of excitatory and inhibitory synaptic inputs results in enhanced visual responses, and with a reduction of spontaneous firing rate, contributes to the maturation of visual cortical RFs. Visual deprivation by dark rearing impedes the normal strengthening of excitatory inputs but leaves the apparently normal enhancement of inhibition while preventing the broadening of the inhibitory subfield, leading to weakened RF responses and a reduced fraction of neurons exhibiting a clear RF, compared with normally reared animals. Our data demonstrate that an experience-dependent and coordinated maturation of excitatory and inhibitory circuits underlie the functional development of visual cortical RFs.SIGNIFICANCE STATEMENT The organization of synaptic RFs is a fundamental determinant of feature selectivity functions in the cortex. However, how changes of excitatory and inhibitory synaptic inputs lead to the functional maturation of visual RFs during cortical development remains not well understood. In layer 4 of mouse V1, we show that a coordinated, balanced enhancement of synaptic excitation and inhibition contributes to the developmental maturation of spatially defined visual RFs. Visual deprivation by dark rearing partially interferes with this process, resulting in a relatively more dominant inhibitory tone and a reduced fraction of neurons exhibiting clear RFs at the spike level. These data provide an unprecedented understanding of the functional development of visual cortical RFs at the synaptic level.     

Excitatory Convergence of Y and Non-Y Information Channels on Single Neurons in the PMLS Area, a Motion Area of the Cat Visual Cortex

We analysed the receptive field properties of neurons in the posteromedial lateral suprasylvian (PMLS) visual cortical area of anaesthetized cats in which there was selective conduction block of the largest (Y-type) fibres in one optic nerve. As in normal cats, in cats with selective block of one optic nerve the great majority of PMLS cells could be activated by photic stimulation through either eye. However, the responses evoked by stimulation via the eye with the selectively pressure-blocked optic nerve ('Y-blocked eye') were significantly weaker than those of the same cells evoked by the stimulation via the normal eye. Accordingly, eye dominance histograms were shifted markedly in favour of the normal eye. Furthermore, there was a significant shift towards lower preferred velocities when PMLS cells were photically stimulated via the Y-blocked eye. Finally, when stimulated via the Y-blocked eye, PMLS cells responded poorly or not at all to high stimulus velocities (≤100°/s). On the other hand, a number of receptive field properties, such as the spatial organization of receptive fields, the size of the discharge fields, orientation tuning and direction selectivity indices, were not significantly affected by the removal of the Y input. We conclude that virtually all neurons in the PMLS area of the cat receive excitatory input from both Y and non-Y information channels, although the Y channel provides the dominant input and makes the principal contribution to the detection of high-velocity motion.     

Receptive‐field properties of V1 and V2 neurons in mice and macaque monkeys

We report the results of extracellular single‐unit recording experiments where we quantitatively analyzed the receptive‐field (RF) properties of neurons in V1 and an adjacent extrastriate visual area (V2L) of anesthetized mice with emphasis on the RF center‐surround organization. We compared the results with the RF center‐surround organization of V1 and V2 neurons in macaque monkeys. If species differences in spatial scale are taken into consideration, mouse V1 and V2L neurons had remarkably fine stimulus selectivity, and the majority of response properties in V2L were not different from those in V1. The RF center‐surround organization of mouse V1 neurons was qualitatively similar to that for macaque monkeys (i.e., the RF center is surrounded by extended suppressive regions). However, unlike in monkey V2, a significant proportion of cortical neurons, largely complex cells in V2L, did not exhibit quantifiable RF surround suppression. Simple cells had smaller RF centers than complex cells, and the prevalence and strength of surround suppression were greater in simple cells than in complex cells. These findings, particularly on the RF center‐surround organization of visual cortical neurons, give new insights into the principles governing cortical circuits in the mouse visual cortex and should provide further impetus for the use of mice in studies on the genetic and molecular basis of RF development and synaptic plasticity. J. Comp. Neurol. 518:2051–2070, 2010. © 2010 Wiley‐Liss, Inc.     

Brain location and visual topography of cortical area V6A in the macaque monkey

The brain location, extent and functional organization of the cortical visual area V6A was investigated in macaque monkeys by using single cell recording techniques in awake, behaving animals. Six hemispheres of four animals were studied. Area V6A occupies a horseshoe-like region of cortex in the caudalmost part of the superior parietal lobule. It extends from the medial surface of the brain, through the anterior bank of the parieto-occipital sulcus, up to the most lateral part of the fundus of the same sulcus. Area V6A borders on areas V6 ventrally, PEc dorsally, PGm medially and MIP laterally. Of 1348 neurons recorded in V6A, 61% were visual and 39% non-visual in nature. The visual neurons were particularly sensitive to orientation and direction of movement of visual stimuli. The inferior contralateral quadrant was the most represented one. Visual receptive fields were also found in the inferior ipsilateral quadrant and in the upper visual field. Receptive fields were on average smaller in the lower visual field than in the upper one. Both central and peripheral parts of the visual field were represented. Large parts of the visual field were represented in small regions of area V6A, and the same regions of the visual field were re-represented many times in different parts of this area, without any apparent topographical order. The only reliable sign of retinotopic organization was the predominance of central representation dorsally and far periphery ventrally. The functional organization of area V6A is discussed in the view that this area could be involved in the control of reaching out and grasping objects.     

Callosal and superior temporal sulcus contributions to receptive field properties in the macaque monkey's nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract.

To assess the functional contribution of the cortical input to the receptive field properties of nucleus of the optic tract (NOT) and dorsal terminal nucleus (DTN) neurons, a first set of experiments evaluated the response properties of NOT-DTN cells in monkeys with split corpus callosum. With respect to visual latency, direction specificity, directional tuning width, velocity tuning, ocular dominance, and binocular interaction, they were indistinguishable from NOT-DTN neurons in normal monkeys. However, a clear difference was found regarding the extent of the receptive fields. Whereas, in normal monkeys, NOT-DTN receptive fields include the contralateral hemifield and the fovea as well as substantial parts of the ipsilateral visual field, receptive fields in callosum-split monkeys stop abruptly at, or close to, the vertical 0-meridian and do not extend into the ipsilateral visual field. In addition, the location of the highest sensitivity within the receptive fields in callosum-split monkeys is shifted away from the vertical 0-meridian in comparison to normal animals. In a second set of experiments, we antidromically identified cortical neurons within the superior temporal sulcus that project to the NOT-DTN. These neurons were found in area MT mostly near the border of MTp or MSTl. All of them are direction selective for ipsiversive stimulus movement, and their receptive fields extend substantially into the ipsilateral visual hemifield. Neurons with other preferred directions did not project to the NOT-DTN. These results contribute to the explanation of the ipsiversive directional deficits in slow eye movements after cortical lesions, as well as the asymmetries in optokinetic nystagmus with hemifield stimulation after transection of the corpus callosum. The more general implication of the results is that a particular function of a cortical area can only be understood by knowing its subcortical connections.     

Functional properties of parietal visual neurons: radial organization of directionalities within the visual field

Parietal visual neurons (PVNs) were studied in waking monkeys as they executed a simple fixation-detection task. Test visual stimuli of varied direction, speed, and extent were presented during the fixation period; these stimuli did not control behavior. Most PVNs subtend large, bilateral receptive fields and are exquisitely sensitive to stimulus motion and direction but insensitive to stimulus speed. The directional preferences of PVNs along meridians are opponently organized, with the preferred directions pointing either inward toward or outward away from the fixation point. Evidence presented in the preceding paper (Motter et al., 1987) indicates that opponent directionality along a single meridian is produced by a feed-forward inhibition of 20 degrees-30 degrees spatial extent. The observations fit a double-Gaussian model of superimposed but unequal excitatory and inhibitory receptive fields: When the former is larger, inward directionality results; when smaller, outward directionality results. We examine here the distribution of the meridional directional preferences in the visual field. Tests showed that opponent organization is not produced by differences in local directional properties in different parts of the receptive field. The distribution of response intensities from one meridian to another is adequately described by a sine wave function. These data indicate a best radial direction for each neuron with a broad distribution of response intensities over successive meridians. Thus, any single PVN, with rare exceptions, cannot signal radial stimulus direction precisely. We then determined how accurately the population response predicted radial stimulus direction by the application of a linear vector summation model. The resulting population vector varied from stimulus direction by an average of 9 degrees. Whether or not the perception of the direction of motion depends upon a population vector remains uncertain. PVNs are especially sensitive to object movement in the visual surround, particularly in the periphery of the visual field. This, combined with their large receptive fields and their wide but flat sensitivity to stimulus speed, makes them especially sensitive to optic flow. This is discussed in relation to the role of the parietal visual system in the visual guidance of projected movements of the arm and hand, in the guidance of locomotion, and in evoking the illusion of vection.