Neuronal Activity in Somatosensory Cortex of Monkeys Using a Precision Grip. I. Receptive Fields and Discharge Patterns

1999 ◽  
Vol 81 (2) ◽  
pp. 825-834 ◽  
Author(s):  
Iran Salimi ◽  
Thomas Brochier ◽  
Allan M. Smith

Neuronal activity in somatosensory cortex of monkeys using a precision grip. I. Receptive fields and discharge patterns. Three adolescent Macaca fascicularis monkeys weighing between 3.5 and 4 kg were trained to use a precision grip to grasp a metal tab mounted on a low friction vertical track and to lift and hold it in a 12- to 25-mm position window for 1 s. The surface texture of the metal tab in contact with the fingers and the weight of the object could be varied. The activity of 386 single cells with cutaneous receptive fields contacting the metal tab were recorded in Brodmann’s areas 3b, 1, 2, 5, and 7 of the somatosensory cortex. In this first of a series of papers, we describe three types of discharge pattern, the receptive-field properties, and the anatomic distribution of the neurons. The majority of the receptive fields were cutaneous and covered less than one digit, and a χ2 test did not reveal any significant differences in the Brodmann’s areas representing the thumb and index finger. Two broad categories of discharge pattern cells were identified. The first category, dynamic cells, showed a brief increase in activity beginning near grip onset, which quickly subsided despite continued pressure applied to the receptive field. Some of the dynamic neurons responded to both skin indentation and release. The second category, static cells, had higher activity during the stationary holding phase of the task. These static neurons demonstrated varying degrees of sensitivity to rates of pressure change on the skin. The percentage of dynamic versus static cells was about equal for areas 3b, 2, 5, and 7. Only area 1 had a higher proportion of dynamic cells (76%). A third category was identified that contained cells with significant pregrip activity and included cortical cells with both dynamic or static discharge patterns. Cells in this category showed activity increases before movement in the absence of receptive-field stimulation, suggesting that, in addition to peripheral cutaneous input, these cells also receive strong excitation from movement-related regions of the brain.

1983 ◽  
Vol 49 (3) ◽  
pp. 804-818 ◽  
Author(s):  
D. G. Tieman ◽  
M. A. McCall ◽  
H. V. Hirsch

1. In order to investigate the effects of an imbalance in stimulation to the eyes without the confounding influence of continuous deprivation of one eye, we reared cats with unequal alternating monocular exposure (AME) and, for comparison, cats with equal AME. We recorded extracellularly from single cells in area 17 of visual cortex. 2. For unequal AME cats, a majority of the cells that were visually responsive were dominated by the eye that had received more patterned visual experience. The percentage of cells dominated by the more experienced eye was greater with a large imbalance in stimulation to the two eyes (AME 8/1, 77%) than with a small imbalance (AME 8/4, 62%). 3. For both equal AME cats and unequal AME cats, we obtained evidence for differences in cells activated by the contralateral and by the ipsilateral afferents. a) In equal AME cats receiving only 1 h of exposure per day, we obtained a greater dominance by the contralateral eye (60%) than in equal AME cats receiving 8 h of exposure per day (42%). b) Although a large imbalance in stimulation (AME 8/1) resulted in a shift in ocular dominance in both cortical hemispheres, a moderate imbalance (AME 8/4) resulted in a smaller shift, which was apparent only in the hemisphere ipsilateral to the less-experienced eye. 4. The percentage of cortical cells responsive to each eye was uniform throughout the depth of cortex. Thus, for the unequal AME cats, cells activated by the less-experienced eye were no more frequent in layer IV of visual cortex than in the infragranular and supragranular layers. 5. Although almost all cells recorded from AME cats had relatively normal receptive-field properties, three receptive-field properties of cells in unequal AME cats showed an effect of the rearing. In each case cells dominated by the less-experienced eye and recorded in the cortical hemisphere ipsilateral to it showed the largest changes. These cells a) were more poorly tuned, b) had lower cutoff velocities, and c) had smaller receptive fields. 6. It is suggested that cortical cells that putatively receive Y-cell afferents from the dorsal lateral geniculate nucleus (LGNd) are more affected by an imbalance in stimulation than are cortical cells that putatively receive X-cell afferents. Thus, the decrease in mean receptive-field area and cutoff velocity for the cells dominated by the less-experienced eye is suggested to be due to a greater shift in ocular dominance by the cortical cells receiving Y-cell afferents from the LGNd. 7. The interaction between binocular competition and deprivation of pattern vision may contribute to differences between monocularly deprived cats and unequal AME cats.


1999 ◽  
Vol 81 (2) ◽  
pp. 835-844 ◽  
Author(s):  
Iran Salimi ◽  
Thomas Brochier ◽  
Allan M. Smith

Neuronal activity in somatosensory cortex of monkeys using a precision grip. II. Responses to object texture and weights. Three monkeys were trained to lift and hold a test object within a 12- to 25-mm position window for 1 s. The activity of single neurons was recorded during performance of the task in which both the weight and surface texture of the object were systematically varied. Whenever possible, each cell was tested with three weights (15, 65, and 115 g) and three textures (smooth metal, fine 200 grit sandpaper, and rough 60 grit sandpaper). Of 386 cells recorded in 3 monkeys, 45 cells had cutaneous receptive fields on the index or thumb or part of the thenar eminence and were held long enough to be tested in all 9 combinations of texture and weight. Recordings were made for the entire anterior-posterior extent of the thumb and index finger areas in somatosensory cortex including area 7b. However, the statistical analysis required a selection of only those cells for which nine complete recording conditions were available limiting the sample to cells in areas 2, 5, and 7b. Significant differences in the grip force accompanied 98% of the changes in texture and 78% of the changes in weight. Increasing the object weight also increased the force tangential to the skin surface as measured by the load or lifting force. The peak discharge during lifting was judged to be the most sensitive index of cell activity and was analyzed with a two-way analysis of variance (ANOVA). In addition, peak cell discharge was normalized to allow comparisons among different combinations of texture and weight as well as comparisons among different neurons. Overall, the peak firing frequency of 87% of the cells was significantly modulated by changes in object texture, but changes in object weight affected the peak activity of only 58% of the cells. Almost all (17/18, 94%) of the static cells were influenced by the object texture, and 81% of the dynamic cells that were active only briefly at grip and lift onset were modulated by texture. For some cells, surface texture had a significant effect on neuronal discharge that was independent of the object weight. In contrast, weight-related responses were never simple main effects of the weight alone and appeared instead as significant interactions between texture and weight. Four neurons either increased or decreased activity in a graded fashion with surface structure (roughness) regardless of the object weight ( P < 0.05). Ten other neurons showed increases or decreases in response to one or two textures, which might represent either a graded response or a tuning preference for a specific texture. The firing frequency of the majority (31/45) of neurons reflected an interaction of both texture and weight. The cells with texture-related but weight-independent activities were thought to encode surface characteristics that are largely independent of the grip and lifting forces used to manipulate the object. Such constancies could be used to construct internal representations or mental models for planning and controlling object manipulation.


Of the many possible functions of the macaque monkey primary visual cortex (striate cortex, area 17) two are now fairly well understood. First, the incoming information from the lateral geniculate bodies is rearranged so that most cells in the striate cortex respond to specifically oriented line segments, and, second, information originating from the two eyes converges upon single cells. The rearrangement and convergence do not take place immediately, however: in layer IVc, where the bulk of the afferents terminate, virtually all cells have fields with circular symmetry and are strictly monocular, driven from the left eye or from the right, but not both; at subsequent stages, in layers above and below IVc, most cells show orientation specificity, and about half are binocular. In a binocular cell the receptive fields in the two eyes are on corresponding regions in the two retinas and are identical in structure, but one eye is usually more effective than the other in influencing the cell; all shades of ocular dominance are seen. These two functions are strongly reflected in the architecture of the cortex, in that cells with common physiological properties are grouped together in vertically organized systems of columns. In an ocular dominance column all cells respond preferentially to the same eye. By four independent anatomical methods it has been shown that these columns have the form of vertically disposed alternating left-eye and right-eye slabs, which in horizontal section form alternating stripes about 400 μm thick, with occasional bifurcations and blind endings. Cells of like orientation specificity are known from physiological recordings to be similarly grouped in much narrower vertical sheeet-like aggregations, stacked in orderly sequences so that on traversing the cortex tangentially one normally encounters a succession of small shifts in orientation, clockwise or counterclockwise; a 1 mm traverse is usually accompanied by one or several full rotations through 180°, broken at times by reversals in direction of rotation and occasionally by large abrupt shifts. A full complement of columns, of either type, left-plus-right eye or a complete 180° sequence, is termed a hypercolumn. Columns (and hence hypercolumns) have roughly the same width throughout the binocular part of the cortex. The two independent systems of hypercolumns are engrafted upon the well known topographic representation of the visual field. The receptive fields mapped in a vertical penetration through cortex show a scatter in position roughly equal to the average size of the fields themselves, and the area thus covered, the aggregate receptive field, increases with distance from the fovea. A parallel increase is seen in reciprocal magnification (the number of degrees of visual field corresponding to 1 mm of cortex). Over most or all of the striate cortex a movement of 1-2 mm, traversing several hypercolumns, is accompanied by a movement through the visual field about equal in size to the local aggregate receptive field. Thus any 1-2 mm block of cortex contains roughly the machinery needed to subserve an aggregate receptive field. In the cortex the fall-off in detail with which the visual field is analysed, as one moves out from the foveal area, is accompanied not by a reduction in thickness of layers, as is found in the retina, but by a reduction in the area of cortex (and hence the number of columnar units) devoted to a given amount of visual field: unlike the retina, the striate cortex is virtually uniform morphologically but varies in magnification. In most respects the above description fits the newborn monkey just as well as the adult, suggesting that area 17 is largely genetically programmed. The ocular dominance columns, however, are not fully developed at birth, since the geniculate terminals belonging to one eye occupy layer IVc throughout its length, segregating out into separate columns only after about the first 6 weeks, whether or not the animal has visual experience. If one eye is sutured closed during this early period the columns belonging to that eye become shrunken and their companions correspondingly expanded. This would seem to be at least in part the result of interference with normal maturation, though sprouting and retraction of axon terminals are not excluded.


1998 ◽  
Vol 80 (6) ◽  
pp. 2882-2892 ◽  
Author(s):  
Christopher I. Moore ◽  
Sacha B. Nelson

Moore, Christopher I. and Sacha B. Nelson. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80: 2882–2892, 1998. Whole cell recordings of synaptic responses evoked by deflection of individual vibrissa were obtained from neurons within adult rat primary somatosensory cortex. To define the spatial and temporal properties of subthreshold receptive fields, the spread, amplitude, latency to onset, rise time to half peak amplitude, and the balance of excitation and inhibition of subthreshold input were quantified. The convergence of information onto single neurons was found to be extensive: inputs were consistently evoked by vibrissa one- and two-away from the vibrissa that evoked the largest response (the “primary vibrissa”). Latency to onset, rise time, and the incidence and strength of inhibitory postsynaptic potentials (IPSPs) varied as a function of position within the receptive field and the strength of evoked excitatory input. Nonprimary vibrissae evoked smaller amplitude subthreshold responses [primary vibrissa, 9.1 ± 0.84 (SE) mV, n = 14; 1-away, 5.1 ± 0.5 mV, n = 38; 2-away, 3.7 ± 0.59 mV, n = 22; 3-away, 1.3 ± 0.70 mV, n = 8] with longer latencies (primary vibrissa, 10.8 ± 0.80 ms; 1-away, 15.0 ± 1.2 ms; 2-away, 15.7 ± 2.0 ms). Rise times were significantly faster for inputs that could evoke action potential responses (suprathreshold, 4.1 ± 1.3 ms, n = 8; subthreshold, 12.4 ± 1.5 ms, n = 61). In a subset of cells, sensory evoked IPSPs were examined by deflecting vibrissa during injection of hyperpolarizing and depolarizing current. The strongest IPSPs were evoked by the primary vibrissa ( n = 5/5), but smaller IPSPs also were evoked by nonprimary vibrissae ( n = 8/13). Inhibition peaked by 10–20 ms after the onset of the fastest excitatory input to the cortex. This pattern of inhibitory activity led to a functional reversal of the center of the receptive field and to suppression of later-arriving and slower-rising nonprimary inputs. Together, these data demonstrate that subthreshold receptive fields are on average large, and the spatio-temporal dynamics of these receptive fields vary as a function of position within the receptive field and strength of excitatory input. These findings constrain models of suprathreshold receptive field generation, multivibrissa interactions, and cortical plasticity.


Contrast sensitivity as a function of spatial frequency was determined for 138 neurons in the foveal region of primate striate cortex. The accuracy of three models in describing these functions was assessed by the method of least squares. Models based on difference-of-Gaussians (DOG) functions were shown to be superior to those based on the Gabor function or the second differential of a Gaussian. In the most general case of the DOG models, each subregion of a simple cell’s receptive field was constructed from a single DOG function. All the models are compatible with the classical observation that the receptive fields of simple cells are made up of spatially discrete ‘on’ and ‘off’ regions. Although the DOG-based models have more free parameters, they can account better for the variety of shapes of spatial contrast sensitivity functions observed in cortical cells and, unlike other models, they provide a detailed description of the organization of subregions of the receptive field that is consistent with the physiological constraints imposed by earlier stages in the visual pathway. Despite the fact that the DOG-based models have spatially discrete components, the resulting amplitude spectra in the frequency domain describe complex cells just as well as simple cells. The superiority of the DOG-based models as a primary spatial filter is discussed in relation to popular models of visual processing that use the Gabor function or the second differential of a Gaussian.


1988 ◽  
Vol 59 (4) ◽  
pp. 1253-1276 ◽  
Author(s):  
R. Metherate ◽  
N. Tremblay ◽  
R. W. Dykes

1. Two-hundred and seven neurons were examined for changes in their responsiveness during the iontophoretic administration of acetylcholine (ACh) in barbiturate-anesthetized cats. 2. The laminar locations of 78 cells were determined. Cholinoceptive neurons were found in all cortical layers and ranged from 50% of the cells tested in layer I to 78% in layer VI. 3. When the responsiveness of a neuron was measured by the magnitude of the discharge generated by a fixed dose of glutamate, 30 of 47 cases (64%) were potentiated, and 4 (8%) were depressed when ACh was administered during glutamate-induced excitation. 4. ACh administered during glutamate excitation was significantly more effective in altering neuronal responsiveness than was ACh administered alone (P less than 0.001). 5. When the responsiveness of a neuron was measured by the magnitude of the discharge generated by a standard somatic stimulus applied to the receptive field, 42 of 52 cases (81%) were potentiated during ACh application. This was again different from ACh treatment alone where only 4 of 27 tests (15%) resulted in subsequent enhancement of the response to somatic stimuli. 6. ACh generally increased the responsiveness of neurons with peripheral receptive fields and caused the appearance of a receptive field in some cells lacking one. 7. In many cases the changes in excitability, as measured by responses either to glutamate or to somatic stimulation, remained for prolonged time periods. When glutamate was used to test excitability, 34% (16 of 47) of the enhancements lasted more than 5 min. When somatic stimuli were used 29% (15 of 52) lasted more than 5 min. With both measures some neurons still displayed enhanced responses more than 1 h after the treatment with ACh. 8. ACh appears to act as a permissive agent that allows modification of the effectiveness with which previously existing afferent inputs drive somatosensory cortical neurons. 9. This mechanism to alter neuronal responsiveness has many of the characteristics necessary to account for the reorganization observed in somatosensory cortex following alterations in its afferent drive and may be related to some forms of learning and memory.


1991 ◽  
Vol 65 (3) ◽  
pp. 572-589 ◽  
Author(s):  
T. M. Wannier ◽  
M. A. Maier ◽  
M. C. Hepp-Reymond

1. Single cell activity was investigated in the precentral motor (MI) and postcentral somatosensory (SI) cortex of the monkey to compare the neuronal activity related to the control of isometric force in the precision grip and to assess the participation of SI in motor control. 2. Three monkeys (Macaca fascicularis) were trained in a visual step-tracking paradigm to generate and precisely maintain force on a transducer held between thumb and index finger. Great care was taken to have the monkeys use only their fingers without moving the wrist or proximal joints. In two monkeys electromyographic (EMG) activity was checked in 23 muscles over several sessions. 3. Five similar classes of task-related firing patterns were found in both SI and MI cortical hand and finger representations, but their relative proportions differed. The majority of the SI neurons were phasically or phasic-tonically active (61%), whereas in MI the neurons that decreased their firing rate with force were most frequent (42%). 4. The timing of activity changes related to the onset of force increase from low to higher levels strongly differed in the two neuronal populations. In SI, only 14% of the task-related neurons increased or decreased their firing rate before the onset of force increase, in contrast to 56% in MI. Only 3% of the SI neurons showed changes before the earliest EMG activation. 5. In both SI and MI neurons with tonic and phasic-tonic, increasing or decreasing discharge patterns disclosed a relationship between neuronal activity and static force. Distinction was made between neurons modulating their activity in a monotonic way and those that were active only at one force level and had a kind of recruitment or deactivation threshold. The latter ones were more frequent in MI than in SI, and in the neuron population with decreasing firing patterns. For the neurons with increases in activity, statistically significant linear correlations between firing rate and force were found more frequently in MI than in SI, where the proportion of nonsignificant correlations was relatively high (35% vs. 15% in MI). In SI the indexes of force sensitivity, calculated from the slopes of the regression lines, covered a wider range than in MI; and their distribution was bimodal, with one mean of 30 Hz/N and the other of 155 Hz/N. In contrast, the mean rate-force slope in MI was 69 Hz/N.(ABSTRACT TRUNCATED AT 400 WORDS)


Perception ◽  
1994 ◽  
Vol 23 (6) ◽  
pp. 691-708 ◽  
Author(s):  
Lothar Spillmann

Psychophysical research on the Hermann grid illusion is reviewed and possible neurophysiological mechanisms are discussed. The illusion is most plausibly explained by lateral inhibition within the concentric receptive fields of retinal and/or geniculate ganglion cells, with contributions by the binocular orientation-specific cortical cells. Results may be summarized as follows: (a) For a strong Hermann grid illusion to be seen bar width must be matched to the mean size of receptive-field centers at any given retinal eccentricity. (b) With the use of this rationale, the diameter of foveal perceptive-field centers (the psychophysical correlate of receptive-field centers) has been found to be in the order of 4–5 min arc and that of total fields (centers plus surrounds) 18 min arc. These small diameters explain why the illusion tends to be absent in foveal vision. (c) With increasing distance from the fovea, perceptive-field centers increase to 1.7 deg at 15 deg eccentricity and then to 3.4 deg at 60 deg eccentricity. This doubling in diameter agrees with the change in size of retinal receptive-field centers in the monkey. (d) The Hermann grid illusion is diminished with dark adaptation. This finding is consistent with the reduction of the center—surround antagonism in retinal receptive fields. (e) The illusion is also weakened when the grid is presented diagonally, which suggests a contribution by the orientation-sensitive cells in the lateral geniculate nucleus and visual cortex. (f) Strong induction effects, similar to the bright and dark spots in the Hermann grid illusion, may be elicited by grids made of various shades of grey; and by grids varying only in chroma or hue. Not accounted for are: the illusory spots occurring in an outline grid ie with hollow squares, and the absence of an illusion when extra bars are added to the grid. Alternative explanations are discussed for the spurious lines connecting the illusory spots along the diagonals and the fuzzy dark bands traversing the rhombi in modified Hermann grids.


1980 ◽  
Vol 43 (6) ◽  
pp. 1673-1699 ◽  
Author(s):  
V. Golovchinsky

1. The responses of single cuneate neurons to controled mechanical stimulation of skin were recorded in cats lightly anesthetized with a nitrous oxide-halothane mixture. The discharge patterns and peripheral receptive-field characteristics were studied in neurons driven by sensitive cutaneous mechanoreceptors, including slowly adapting skin mechanoreceptors. Virtually all cuneate neurons display maximum discharge during the velocity component of displacement. 2. Among cuneate neurons encountered in this study, approximately 46% were driven by guard hair mechanoreceptors, 15% were driven by field receptors, and 13% were driven by slowly adapting skin receptors. Neurons responding to stimulation of deep tissues (including claws) were not studied with controlled mechanical stimulation and accounted for 19%. The rest of the neurons were driven by Pacinian corpuscles, received afferent inputs from several different first-order afferents, or were not definitely identified. There was no clear evidence of down hair or high-threshold mechanoreceptor representation. 3. The discharge pattern in response to a constant-velocity stimulus proved most valuable in describing submodality classes of neurons driven by hair and field receptors since sensitivity of these neurons to dynamic and to static phases of stimulation constitute respective continua and, thus, preclude sharp separation into distinct groups. 4. The majority of neurons displayed response properties and receptive fields similar to those of first-order afferents. A minority of cells had receptive fields that were larger than those of primary afferents, with nearly identical modality and velocity characteristics throughout the receptive field. 5. Approximately 2% of recorded neurons displayed convergent properties not encountered in first-order afferents, including neurons driven from receptors of different modalities or from discontinuous receptive fields. 6. Inhibition of neuronal firing generated from outside the receptive field was rarely seen, possibly due to anesthetic conditions. In a small number of neurons, irregularities in the discharge were observed that might indicate inhibitory influences originating from within the receptive field.


1991 ◽  
Vol 65 (2) ◽  
pp. 178-187 ◽  
Author(s):  
M. B. Calford ◽  
R. Tweedale

1. Acute effects of permanent and temporary denervation of the flying fox thumb were examined to test the hypothesis that a large area of skin around the cutaneous receptive field of multiunits (MRF) at a locus in primary somatosensory cortex (SI) supplies viable inputs which can be rapidly unmasked by interruption of the dominant input from the area of the MRF. 2. The immediate effect of amputation of the thumb at loci where the original receptive field was entirely removed was to produce large MRFs on adjacent body areas (wrist, forearm, prowing, and finger membranes). Greatly expanded MRFs were also produced when amputation removed only part of the original MRF at a cortical locus. 3. The probable source of input to account for the new receptive fields is the extensive arborization of ascending projections within the somatosensory pathway, which supply a cortical locus with a potential input from a far larger area than is represented in its normal receptive field. The rapidity with which new or expanded fields are seen following denervation indicates that the normally unexpressed inputs around a receptive field are not only potential inputs but are inherently viable. Hence the most likely explanation for the results of this study is that the effect of the denervation is to disrupt an inhibitory influence that normally has the role of shaping the receptive field. 4. Temporary anesthesia of all or part of a MRF produced similar initial effects to amputation. When responsiveness returned to the locally anesthetized area (after 10-30 min), an expanded MRF persisted for a short time after which the boundaries of the MRF shrank. This rapid reversal suggests that a mechanistic rather than a plastic change is the basis for the acute effect of a small denervation on SI.


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