Unit activity in monkey parietal cortex related to haptic perception and temporary memory

SummaryThe neural responses of 456 single units were recorded in parietal cortex of behaving monkeys during a haptic delayed matching-to-sample task. (1) In areas 2 and 5 together, 22% of the neurons were activated by the auditory cue that signalled the beginning of a trial. Virtually all of these cells were also activated during the arm movements required by the task. These neurons, showing both auditory-related and movement-related responses, may function in sensorimotor integration. (2) Responses related to arm projection frequently began before movement onset, sometimes as much as 320 ms before. Such “premovement” responses were approximately equally common, and showed the same latency distribution, in areas 2, 5a, and 5b. (3) There was a topographic rostral-to-caudal gradient of decreasing neural responsiveness to the animal's manipulation of the cue (sample) objects. Eleven percent of manipulation-activated cells responded preferentially to one of the sample objects. (4) Many cells showed sustained (> 3 s) activation during the delay period (the time between handling of the sample object and palpation of the choice objects), even though at that time the monkey was sitting quietly and without stimulation. (5) Cells with sustained activation throughout most or all of the 18-s delay period were rare in all areas tested except area 5a. These cells, especially those that were preferentially activated depending on which sample object was palpated, may function in the temporary retention of haptic attributes. (6) The population of cells activated during sample manipulation was largely distinct from the population of cells showing sustained activation during the delay period. These two cell populations may represent different but complementary aspects of haptic perception. (7) The most common response during the delay period was sustained inhibition. This may be an expression of a nonspecific mechanism for decreasing background noise and enhancing neural responses to an anticipated perceptual event. (8) Relatively little evidence was found to support a functional distinction between the neural response properties of areas 2 and 5 a. This suggests that area 2 may be at a higher level in the somatosensory heirarchy of the posterior parietal cortex than usually considered.

[1]  Louis W. Gellermann Chance Orders of Alternating Stimuli in Visual Discrimination Experiments , 1933 .

[2]  Cranio-cerebral topography of the monkey , 1945 .

[3]  R. Galamboš,et al.  Extralemniscal activation of auditory cortex in cats. , 1961, The American journal of physiology.

[4]  J. Gibson The Senses Considered As Perceptual Systems , 1967 .

[5]  K. Bignall,et al.  Nonprimary sensory projections on the cat neocortex. , 1967, International review of neurobiology.

[6]  T. Powell,et al.  Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions. , 1969, Brain : a journal of neurology.

[7]  H. W. Bond,et al.  Solid miniature silver-silver chloride electrodes for chronic implantation. , 1970, Electroencephalography and clinical neurophysiology.

[8]  F. Duffy,et al.  Somatosensory System: Organizational Hierarchy from Single Units in Monkey Area 5 , 1971, Science.

[9]  H. Sakata,et al.  Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. , 1973, Brain research.

[10]  C. Gross Visual Functions of Inferotemporal Cortex , 1973 .

[11]  J. Hyvärinen,et al.  Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys. , 1974, Brain : a journal of neurology.

[12]  E V Evarts,et al.  Precentral and postcentral cortical activity in association with visually triggered movement. , 1974, Journal of neurophysiology.

[13]  J. Semmes,et al.  Behavioral consequences of selective subtotal ablations in the postcentral gyrus of Macaca mulatta. , 1974, Brain research.

[14]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[15]  Michio Tanaka,et al.  Postcentral neurons in hand region of area 2: their possible role in the form discrimination of tactile objects , 1978, Brain Research.

[16]  Juhani Hyva¨rinen Regional distribution of functions in parietal association area 7 of the monkey , 1981, Brain Research.

[17]  J. Fuster,et al.  Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. , 1981, Science.

[18]  J Hyvärinen,et al.  Regional distribution of functions in parietal association area 7 of the monkey. , 1981, Brain research.

[19]  D. Pandya,et al.  Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey , 1982, The Journal of comparative neurology.

[20]  J. Seal,et al.  Activity of neurons in area 5 during a simple arm movement in monkeys before and after deafferentation of the trained limb , 1982, Brain Research.

[21]  J. Fuster,et al.  Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks , 1982, Experimental Neurology.

[22]  J M Fuster,et al.  Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  Roger Salamon,et al.  A statistical method for the estimation of neuronal response latency and its functional interpretation , 1983, Brain Research.

[24]  Christian Gross,et al.  Instruction-related changes of neuronal activity in area 5 during a simple forearm movement in the monkey , 1983, Neuroscience Letters.

[25]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.

[26]  R. Bauer,et al.  Short-term memory for haptic cues in monkeys (Macaca mulatta) , 1985 .

[27]  Masahiro Sakamoto,et al.  Functional surface integration, submodality convergence, and tactile feature detection in area 2 of the monkey somatosensory cortex , 1985 .

[28]  J. Kaas,et al.  The somatotopic organization of area 2 in macaque monkeys , 1985, The Journal of comparative neurology.

[29]  Joaquin M. Fuster,et al.  The elgiloy microelectrode: Fabrication techniques and characteristics , 1985, Journal of Neuroscience Methods.

[30]  A. P. Georgopoulos,et al.  Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex , 1983, Experimental Brain Research.