Receptive-field transformations between LGN neurons and S-cells of cat-striate cortex.
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Biomedical subjects
Publications and source records attributed to G H Henry.
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From the extracellular recording of single units in the monkey striate cortex and electrical stimulation at two selected sites in the optic radiations it was possible to estimate 1) the ordinal position of striate neurons (i.e., whether they received a monosynaptic, disynaptic or polysynaptic input from the thalamus) and 2) the nature of the afferent input to these neurons (i.e., whether it came from the magnocellular or parvocellular subdivision of the lateral geniculate nucleus (LGN)). Based on receptive field properties six major classes of striate neuron were identified--three which lacked orientation specificity (the ON-center, the OFF-center, and the ON/OFF or nonoriented (N-0) receptive fields) and three with orientation specific responses (the S, the C, and the B categories of receptive field). Units lacking orientation specificity were concentrated in laminae 4A, 4C beta and 6 while, for the cells with orientation specificity, C cells were found in laminae 4B and 6, B cells in 2/3 and 5, and S cells predominantly in laminae 2/3, 4C alpha, and 5. The results of electrical stimulation indicated that cell-to-cell transmission time in the monkey striate cortex is 1.5 msec, and latency measures showed that cells with a monosynaptic drive from the thalamus were confined to laminae 4 and 6 while disynaptically driven cells were found principally in upper lamina 4 (4A and 4B). No cell class was identified exclusively with a given ordinal position and there were many types of potential first-order neurons. The conduction time from one stimulating electrode to the next in the optic radiation was used to identify the afferent input to each striate neuron. The input to color-coded neurones was found to come exclusively from parvocellular layers while the C cells and two subclasses of the S cell (S2 and S3) were driven predominantly by the magnocellular subdivision. For other cell types (those with ON-center, N-0, and S1 receptive fields) the input came from either type of LGN neuron. The laminar distribution of neurons receiving a direct input from the magnocellular and parvocellular streams is in accord with the results of anatomical studies into the site of termination of the LGN input. The cell types receiving these direct inputs vary in the two streams so that the parvocellular input terminates on cells with ON-center and N-0 receptive fields in lamina 4C beta while the magnocellular input goes to cells with S, ON-center, N-0, and C receptive fields in lamina 4C alpha and the lower part of 4B. Consideration is given to the influence of these results on models for neural processing in monkey striate cortex and a comparison is drawn with the results of similar studies in the cat.
A simple device for injecting horseradish peroxidase into the cerebral cortex is described. It consists of a syringe connected by tubing to a hydraulic adaptor which provides a sealed connection to a disposable glass micropipette. Replaceable micropipettes may be prepared by drawing capillary glass under heat to a fine diameter tip that provides easy penetration into the cortex without dimpling the surface grey matter or damaging the underlying white matter. The hydraulic seal achieved by the adaptor allows volumes of the order of 0.05 microliter to be readily injected into nervous tissue.
A laminar distribution of different functional cell types in the striate cortex of the cat is drawn up from the visual responses of single cells recorded in 64 electrode penetrations in 38 cats. In summary, S cells were found to be concentrated in laminae 4 and 6; SH cells in laminae 2, 3 and 4; C cells in laminae 5 and lower 3; B cells in laminae 3 and upper 5 and cells with non-oriented receptive fields in lamina 4. In addition, the nature of afferent innervation to striate neurons was derived from the latency of the orthodromic response to electrical stimulation in the optic chiasm and optic radiations in 19 cats. An analysis of latency values allowed the afferent innervation to a cell to be classed as belonging either to fast or slow conducting streams in the population of dLGN axons and also permitted a decision to be made on whether or not the afferent path passed directly to the cell. Direct afferent innervation from the dLGN was not found to be confined to a single class of striate neuron. Instead, examples of cells with S, SH, C, B and non-oriented receptive fields all had orthodromic latencies that met the requirement for direct innervation. Instances of cells with orthodromic latencies suggestive of indirect innervation were also found for most receptive field classes but these cells were encountered less frequently than those with a direct afferent input. It is argued that a variety of different cell types may act as first order neurons in the striate cortex and that cells occurring at later stages in the sequence of cortical processing may have been incompletely studied because they are more difficult to stimulate either visually or electrically.
Golgi and axonal transport techniques have been used to examine the organization of neurons within primary visual cortex, area 17, of the cat. This organization has been compared to that of the primate cortical area 17 as described in previous studies and it is discussed in relationship to the distribution of afferents from the dorsal lateral geniculate nucleus (dLGN). The visual cortex of the cat and monkey show strong similarities in the laminar positions of neurons projecting extrinsically and also in the restriction of spiny stellate neurons to a central lamina (lamina 4) receiving input from the dLGN. However, lamina 4B in the monkey, which contains spiny stellate neurons but does not receive direct input from the dLGN, has no direct counterpart in cat area 17. Axon projections of spiny stellate neurons in the other divisions of lamina 4 differ in cat and monkey: the small, closely packed neurons in the lowermost division of lamina 4 (4B in the cat, 4Cbeta in the monkey) project chiefly within lamina 4 in the cat whereas in the monkey they have a strong projection to lamina 3. In the cat, spiny stellate neurons of lamina 4A project upon lamina 3 whereas in the monkey those in the apparently equivalent zone, 4Calpha, project upon lamina 4B. Most non-spiny stellate neurons examined have precisely organized interlaminar axonal projections which differ from the axon trajectories of neighboring spiny neurons.
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Spatial summation of responses in striate neurons in cats under N2O/O2 anaesthesia was examined quantitatively both along the line of the optimal stimulus orientation (length summation) using moving light bars and single light and dark edge stimuli, and at right angles to the optimal orientation (width summation) using stationary flashing bars. Activity profiles and length-response curves were prepared from simple, complex and hypercomplex I and II cells. An activity profile indicates the responsiveness of a cell at locations along the length of its receptive field. The activity profiles from all cell types were usually well fitted by Gaussian functions. Length summation occurs both in end-free (simple and complex) and, to a lesser extent, in end-stopped (hypercomplex I and II) cells over a wide range of stimulus contrasts (0.13 to 0.95). The linearity of length summation was tested either by comparing the recorded length-response curves with the curves predicted from the linear integration of the activity profiles or by comparing the response to the activation of two regions of the receptive field with the sum of the responses to each region activated separately. Although length summation was usually non-linear (either greater than or less than direct proportionality) it was more nearly linear in complex than it was in simple and hypercomplex I cells. Mechanisms responsible for non-linear length summation were studied, including a threshold for discharge, response saturation and summation of end-zone inhibition. Complex cells show little width summation for bars wider than 0.3 degrees. In simple and hypercomplex I cells there was also relatively little width summation either in an ON or an OFF discharge region at contrasts above about 0.4 but at lower contrasts width summation may be apporximately linear. Spatial summation of responses does not appear to be a useful characteristic for distinguishing one striate cell type from another.
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1. Using a multi-histogram technique forty-seven response-velocity curves were prepared for a variety of visual stimuli presented to twenty-one cells in the striate cortex of the anaesthetized, paralysed cat. 2. The character of each velocity-response curve varied according to the measurement used in assessing a response. Reasons are advanced for sampling the response over a single bin of short duration at the peak of the discharge in each average response histogram. 3. The sharpness of tuning varied markedly throughout the population of cells but it was not possible to establish any definitive class differences. 4. For simple and complex cell categories there was considerable overlap in both the range of effective stimulus velocities and the distribution of the optimal velocities. An observation not emphasized in the past was that some simple cells responded to very fast stimuli while a number of complex cells were driven by very slowly moving stimuli. 5. Generally changes in stimulus parameters such as the polarity of contrast of a moving edge, its orientation or direction of movement produced only slight modifications in the profile of the velocity-response curve. 6. The abolition of the response of simple cells that failed to be driven by rapidly moving stimuli was shown to be due to the entry of the stimulus into the inhibitory flank distal to the discharge region. When the movement of the stimulus was confined to the discharge region there was little evidence of velocity dependence in the response. The duration over which the inhibition from the distal flank remained effective was evaluated for representative simple cells.
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Most simple cells in the striate cortex of the cat are direction selective, firing to broadside movement of an optimally oriented edge or bar in one direction of motion and not the other. The smallest stimulus displacement for which a direction-selective discrimination can be made cannot be smaller than the threshold for the detection of the displacement itself. It is shown that retinal image quality is an important limiting factor in respect to the thresholds both for stimulus displacement and direction selectivity.
Following our earlier study on direction selectivity in simple cells (5), the present findings on complex cells made it possible to compare the direction selectivity in the two types of striate cell. Common properties were found in the dimension of the smallest stimulus displacement giving a direction-selective response and in the role of inhibition in suppressing the response as the stimulus moved in the nonpreferred direction. However, the effectiveness of this inhibition varied in the two cell types since it suppressed both driven and spontaneous activity in the simple cell, but only driven firing in the complex cell. It is argued that direction selectivity must enter the response before the complex cell if the inhibition responsible for it's generation fails to influence the spontaneous activity of the cell. The consequences of this finding are considered in the terms of parallel or sequential processing of visual information in striate cortex.
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