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V B Mountcastle

Publications and source records attributed to V B Mountcastle.

At least 19 recordsLinked to original sources

The columnar organization of the neocortex.

The modular organization of nervous systems is a widely documented principle of design for both vertebrate and invertebrate brains of which the columnar organization of the neocortex is an example. The classical cytoarchitectural areas of the neocortex are composed of smaller units, local neural circuits repeated iteratively within each area. Modules may vary in cell type and number, in internal and external connectivity, and in mode of neuronal processing between different large entities; within any single large entity they have a basic similarity of internal design and operation. Modules are most commonly grouped into entities by sets of dominating external connections. This unifying factor is most obvious for the heterotypical sensory and motor areas of the neocortex. Columnar defining factors in homotypical areas are generated, in part, within the cortex itself. The set of all modules composing such an entity may be fractionated into different modular subsets by different extrinsic connections. Linkages between them and subsets in other large entities form distributed systems. The neighborhood relations between connected subsets of modules in different entities result in nested distributed systems that serve distributed functions. A cortical area defined in classical cytoarchitectural terms may belong to more than one and sometimes to several distributed systems. Columns in cytoarchitectural areas located at some distance from one another, but with some common properties, may be linked by long-range, intracortical connections.

Animals↗

Adaptation of the Reitboeck method of multiple microelectrode recording to the neocortex of the waking monkey.

We adapted to the neocortex of waking monkeys a method for multiple microelectrode recording devised by Reitboeck. A sliding platform allows micropositioning of 7 electrodes independently, in 2 microns steps. Microelectrodes are quartz glass filaments (80 microns o.d.) with central metal cores (30 microns) of tungsten-platinum alloy. Filaments are drawn in a high temperature chamber, and ground to the desired form and tip size. The microdrive is held over the region to be explored, and the microelectrodes passed through 300 microns o.d. guide tubes fixed in implant thimbles of chosen size an and x - y arrangement of tubes, sealed by an O-ring into a small craniotomy opening. A microprocessor controlled recording system provides gain, noise and wave-shape filtering, impedance testing, and differential amplitude discrimination for each channel. Electrode movement is obtained via the microprocessor which displays and updates on the console terminal the electrode depth, impedance, and the channel assignment of each electrode. A second microprocessor based system is used to collect, buffer, and encode in real time all event data, which are transferred whenever convenient to a minicomputer that controls the experiment. Exploratory recordings were made in the posterior parietal, somatic sensory, and motor cortical areas. The system has now been used successfully in a number of investigations.

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Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeys.

The capacities of humans and monkeys to discriminate between the frequencies of mechanical sinusoids delivered to the glabrous skin of the hand have been measured in psychophysical experiments. The 2 primates have similar capacities; they make discriminations with Weber fractions that change little over the frequency range from 20 to 200 Hz. The discriminatory capacities are similar whether stimuli are received passively or acquired actively. Combined experiments have been made in monkeys in which the electrical signs of the activity of quickly adapting (QA) and slowly adapting (SA) neurons of postcentral areas 3b and 1 were recorded, both in the working state as the animal made discriminations and in the irrelevant state in which the stimuli did not guide behavior. The neuronal responses were analyzed in terms of discharge rates, periodicities in the neuronal discharges, and harmonic contents. It was shown that discriminatory capacity depends upon the period lengths in the sets of periodically entrained activity evoked by stimuli readily discriminated, and not upon the small differences in rates of discharge evoked by those stimuli. The periodicities were shown by harmonic analysis to be sharply limited to stimulus frequencies. Low-frequency stimuli evoke periodicities at the second and third harmonics in some neurons, in addition to strongly periodic signals at the fundamental frequency of the stimuli. Their presence does not appear to interfere with frequency discrimination. Neuronal responses recorded in the stimulus-irrelevant state were not distinguishable from those recorded as monkeys made discriminations. The responses of SA neurons, recorded under similar conditions, resembled those of QA neurons in almost every feature, but reasons are given for concluding that the SA system plays no role in frequency discrimination in the sense of flutter.

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Common and differential effects of attentive fixation on the excitability of parietal and prestriate (V4) cortical visual neurons in the macaque monkey.

The excitability of cortical neurons of prestriate area V4 and area PG of the inferior parietal lobule were examined using the method of single-neuron analysis in awake macaque monkeys. Levels of excitability were measured as the intensity of response to optimal visual stimuli placed in the most responsive region of the cell's receptive field. Physically and retinotopically identical stimuli were delivered during eye movement pauses under 3 conditions: during a no-task state in which the animal was awake and alert, but not receiving or expecting rewards or working in any task; between trials of the task state, the intertrial interval, while the animal awaited the appearance of a fixation target; and during the foreperiod of the task state, as the animal attentively fixated a small target light, waiting to detect its dimming in order to receive liquid reward. Experiments were carried out in 6 hemispheres of 4 monkeys; both V4 and PG were examined through the same chamber placements in 2 hemispheres. A total of 478 neurons in V4 and PG were identified as visual; quantitative studies were done on 146 in V4 and 54 in PG. We found in these experiments a common effect, a 3-4-fold facilitation of the responses of both V4 and PG visual neurons during the task state as compared to in the no-task state, and a differential effect, in that V4 neurons showed a similar 3-4-fold facilitation of responses to stimuli presented during the intertrial interval, whereas PG neuronal responses during this interval were similar to those evoked in the no-task state. We describe the functional properties of V4 neurons studied in the waking state. The findings are discussed in relation to the positions of these 2 areas in the occipitoparietal and occipitotemporal transcortical visual systems and to their respective roles in visuospatial perception and pattern recognition. They are also discussed with regard to the candidate neural mechanisms through which the changes in cortical neuronal excitability might be mediated.

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Functional properties of parietal visual neurons: mechanisms of directionality along a single axis.

The directional properties of parietal visual neurons (PVNs) were examined using the method of single-neuron analysis in waking monkeys. PVN properties were determined with passive visual stimuli as the animal executed a simple detection task. Parietal area PG was studied in 10 hemispheres of 6 male Macaca mulatta. Each class of parietal neurons was identified in PG: the fixation, projection, visual, and oculomotor neurons; 613 PVNs were identified, 323 were studied quantitatively, and 188 were studied with one or more of the protocols described. The receptive fields of PVNs are commonly large and bilateral, and at the limit some may fill the visual field; for many, the central zone of the visual field is spared when the fields are determined by stimuli that enter from the periphery and transit meridians. The receptive fields vary with the behavioral state, the angle of gaze, and the parameters of the stimuli used to determine them. PVNs are sensitive to stimulus movement but relatively insensitive to stimulus speed; many respond over a speed range of 5 degrees-500 degrees/sec. Stimulus-response relations may be incremental or decremental with increasing speed or show maxima or minima in the midrange of speed, but the response variation over the full range is rarely greater than 2:1. The directional preferences of PVNs with bilateral receptive fields are opponently organized; the preferred directions point either inward toward or outward away from the central line of gaze along the 4 meridians tested, which were equally spaced in the circular dimension of the visual field. The mechanism of the axis directionality of PVNs was studied using conditioning-test paradigms. They revealed a feed-forward inhibition preceding a stimulus, an effect that extends from the leading edge of the stimulus for 10 degrees-20 degrees in front of the moving stimulus and lasts for several hundred milliseconds. A double-Gaussian model of superimposed but unequal excitatory and inhibitory effects suffices to explain the present observations. It places demand upon the projection of functional properties from the contralateral hemisphere or from the ipsilateral prestriate areas that project upon PG over multistaged pathways and minimal demands upon intracortical processing mechanisms.

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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.

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The influence of the angle of gaze upon the excitability of the light-sensitive neurons of the posterior parietal cortex.

The responses of parietal visual neurons are markedly increased during attentive fixation, as compared to those evoked in relaxed wakefulness, an effect specific for directed attention and unrelated to putative differences in the general level of arousal. Those responses are also strongly influenced by the angle of gaze, an effect observed only during directed visual attention. The change in response is smoothly graded along a meridian for about one-half the neuron population; the average spatial gradient from maximum to minimum is 78% response for a 20 degrees shift in eye position. No lateral preference was observed. For the remaining half, responses were either maximal or minimal for fixations dead ahead, and changes occurred with deviations in any direction. Angle of gaze effects were observed for neurons with foveal as well as eccentrically located receptive fields, all of which were organized in retinotopic not spatial coordinates. Control experiments showed that the effect was not produced by changes in visual background with changes in the angle of gaze, nor to changes in fixation distance, nor to variations in the intensity of stimuli viewed from different angles. The effect depends upon the position of the eye in the orbit, but is unlikely due to a direct central action of changes in nonretinal orbital afferent activity at different angles of gaze, for the effect was rarely observed with changes in the angle of gaze during relaxed wakefulness without directed visual attention. The evidence supports the interpretation that the effect is produced by a central influence of the systems controlling directed visual attention and the angle of gaze upon those linking the retinae to the parietal lobe.

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The influence of attentive fixation upon the excitability of the light-sensitive neurons of the posterior parietal cortex.

We describe the effect of behavioral state upon the excitability of light-sensitive (Ls) neurons of the inferior parietal lobule, area 7a, studied in waking monkeys. The responses of parietal LS neurons to visual stimuli are facilitated during the state of attentive fixation of a target light as compared to their responses to physically and retinotopically identical test stimuli delivered during the eye pauses of alert wakefulness. Seventy percent of the neurons tested (n = 55) showed significant increments in responses in the state of attentive fixation; the median value of the increments was 3.5 times. Only 4 of the 55 cells examined completely showed the reverse relation. Three sets of control experiments were done. The facilitation occurred when the responses evoked during the trials of a reaction task with attentive fixation of a target were compared with those evoked by identical stimuli delivered to the same retinotopic locations at the end of each intertrial interval: the facilitation of attentive fixation is not due to a shift in the general level of arousal. The facilitation occurred when the animal maintained attentive fixation of a spot of the tangent screen without a target light or when an additional light mimicking the target light was presented along with testing stimuli in the state of alert wakefulness without attentive fixation: the facilitation is not produced by a sensory-sensory interaction between target and testing lights. Finally, the facilitation was observed whether or not the test stimuli were behaviorally relevant. We conclude that the act of attentive fixation exerts a specific and powerful effect upon the excitability of the neural systems linking the retinae and the inferior parietal lobule and that the facilitation plays an important role in visually guided behavior.

Animals↗

The functional properties of the light-sensitive neurons of the posterior parietal cortex studied in waking monkeys: foveal sparing and opponent vector organization.

We describe in this paper the results of a new study of the inferior parietal lobule in 10 waking monkeys combining the methods of behavioral control, visual stimulation, and single neuron analysis. In this study, 1682 neurons were identified; 804 were studied in detail. Neurons insensitive to visual stimuli comprise the fixation, oculomotor, and projection-manipulation classes thought to be involved in initiatives toward action. The largest group of the light-sensitive (LS) neurons were activated from large and frequently bilateral response areas that excluded the foveal region; we term this foveal sparing. The remaining cells subtended areas including the fovea, when tested with large stimuli (6 degrees X 6 degrees), but only 8 of 216 cells studied in detail responded to the small fixation target light. We propose that a dynamic central neural process associated with the acts of fixation and visual attention suppresses responses to foveal stimuli. Parietal LS neurons are sensitive to stimulus movement and direction over a wide range of velocities. The vectors point either inward toward the center or outward toward the perimeter of the visual field, and for neurons with bilateral response areas, the vectors commonly point in opposite directions in the two half-fields; we term this opponent vector organization. The functional properties of area 7 LS neurons are such that they could signal motion in the immediate surround and the apparent motion accompanying head movements and forward locomotion. We surmise that they contribute to a central neural image of immediately surrounding space and to the perceptual constancy of that space obtaining during bodily movement. These properties are suitable for the attraction of gaze and attention to objects and events in the peripheral visual fields. It is this system, together with the classes of parietal neurons concerned with action initiatives, whose destruction is thought to account for the hemi-inattention and neglect of the parietal lobe syndrome in primates.

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Disorders in somesthesis following lesions of parietal lobe.

1. We determined the effects of lesions of the parietal lobe on the capacities of monkeys to detect and discriminate between mechanical sinusoids delivered to the hand. Tests of discrimination measured the capacity to discriminate between frequencies of flutter (24--36 Hz) and the capacity to make gross discriminations of frequency of flutter-vibration over the range of 10--50 Hz. 2. A unilateral removal of the parietal lobe impaired sensory capacities only on the contralateral hand; detection threshold was elevated, the capacity to discriminate between frequenceis of flutter was permanently lost, and the capacity to discriminate between and identify frequencies of 10--50 Hz was grossly impaired. No defects were found on the hand ipsilateral to the lesion. Detection thresholds, but not discrimination thresholds, decreased during postoperative testing, but in most cases did not recover to preoperative values. The impairments in frequency discrimination remained through the last day of postoperative testing. 3. A unilateral, subtotal parietal lesion that completely destroyed the primary and secondary somatic areas and Brodmann's area 5 resulted in the same sensory impairments as those produced by total removal of the parietal lobe. In most cases, detection threshold was elevated; flutter-frequency discrimination was lost, and the capacity to discriminate between frequencies of 10--50 Hz over the extended range of flutter and vibration was impaired. 4. The loss in discriminative capacity following lesions of the somatosensory cortex is interpreted as due to the absence of a cortical mechanism that determined differences in the temporal pattern of cyclically entrained activity in the somatic afferent pathway. This loss was dissociated from the remaining capacity, although impaired, to detect the presence of any neural activity in the afferent pathways or to determine gross differences in the frequency of mechanical sinusoids by a mechanism of coding by the labeled line.

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Mechanisms of neural integration in the parietal lobe for visual attention.

The impulse discharges of neurons in the inferior parietal association cortex (area 7) were studied in the alert, behaving rhesus monkey, trained to fixate and follow visual targets. Four classes of cells related to visual or visuomotor function were found. Cells of one of these are sensitive to visual stimuli and have large, contralateral receptive fields with maximal sensitivity in the far temporal quadrants. Cells of the other three classes are related to visuomotor functions: visual fixation, tracking, and saccades. They are neither sensory nor motor in the usual sense for they are activated only by interested fixation of gaze or tracking, or before visually evoked saccadic eye movements. They are not activated during the spontaneous saccades and fixations that the monkey makes while casually exploring his environment. It is hypothesized that the light-sensitive neurons provide the visual input to the visuomotor cells that, in turn, produce a command signal for the direction of visual attention and for shifting the focus of attention from one target to another.

Animals↗

Visual input to the visuomotor mechanisms of the monkey's parietal lobe.

A newly identified class of neurons of the parietal cortex, studied in waking monkeys (Macaca mulatta), is activated by visual stimuli, perhaps via the retino-collicular visual pathway. This afferent input is thought to provide the visual cues activating the visuomotor mechanisms of the parietal lobe for the direction of visual attention.

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Parietal lobe mechanisms for directed visual attention.

1. Experiments were made on the cortex of the inferior parietal lobule in 10 hemispheres of six alert, behaving monkeys. The electrical signs of the impulse discharges of single cortical cells were recorded as the monkeys executed tasks requiring them to fixate stationary visual targets, track those which moved slowly, and to make saccadic movements to foveate those which suddenly jumped from one locus to another within the field of view. A total of 907 neurons of area 7 were identified in terms of their physiological properties, particularly the correlation of their activity with the oculomotor components of these behavioral acts of directed visual attention; 480 of these were located by cytoarchitectural layer. Most identifiable cells of area 7 are visuomotor neurons, in a special and conditional sense. Their discharge frequencies increase before and during those steady fixations and movements of the eyes which secure and maintain foveation of objects, but only if the visual targets engaged are linked by a strong motivational drive; in our experiments, one between thirst and the light whose dimming the animal has learned to detect for liquid reward. We have identified and studied three major classes of neurons in area 7. 2. The visual fixation neurons (57%) accelerate discharge synchronously with fixation of a visual object the animal desires. The incremented discharge continues until reward, but then declines abruptly even when there is no immediate shift of the line of gaze. Fixation neurons are relatively inactive during those casual fixations by which the animal insepcts the surrounding environment. Mist fixation neurons subtend gaze fields limited to one quadrant or half of the total gaze field. The sum of the gaze fields of the fixation neurons in one hemisphere is weighted moderately toward the contralateral side. Fixation cells also discharge during slow pursuit movements in any direction so long as the movement stays within the gaze field of the neuron under study. About 40% of fixation cells are suppressed before and during saccadic movements of the eyes to a new target within the gaze field of the fixation cell. Those suppressed are located preferentially in layer V of the cortex. Suppression is maximal for saccades directed contralaterally to the hemisphere under study. 3. Visual tracking neurons are active during oculomotor pursuit of slowly moving visual objects, not during steady fixations. They show a marked directional but no laterality relation, and are suppressed before and during a visually evoked saccade superimposed on the smooth pursuit movement. The rate of discharge is a flat function of tracking speed so that these cells do not appear to emit signals which specify the speed of smooth pursuit movements. 4. The saccade neurons are active before and during visually evoked saccadic movements of the eyes but not before spontaneous saccades, no matter whether made in light or near darkness. The discharge of saccade neurons leads the eye movement by as much as 150 ms (mean, 73 ms)...

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