Anterior parietal cortical response to tactile and skin-heating stimuli applied to the same skin site.

1. The response of anterior parietal cortex to skin stimuli was evaluated with optical intrinsic signal imaging and extracellular microelectrode recording methods in anesthetized squirrel monkeys. 2. Nonnoxious mechanical stimulation (vibrotactile or skin tapping) of the contralateral radial interdigital pad was accompanied by a decrease in reflectance (at 833 nm) in sectors of cytoarchitectonic areas 3b and 1. This intrinsic signal was in register with regions shown by previous receptive field mapping studies to receive low-threshold mechanoreceptor input from the radial interdigital pad. 3. A skin-heating stimulus applied to the contralateral radial interdigital pad with a stationary probe/thermode evoked no discernable intrinsic signal in areas 3b and 1, but evoked a signal within a circumscribed part of area 3a. The region of area 3a responsive to skin heating with the stationary probe/thermode was adjacent to the areas 3b and 1 regions that developed an intrinsic signal in response to vibrotactile stimulation of the same skin site. Skin heating with a stationary probe/thermode also evoked intrinsic signal in regions of areas 4 and 2 neighboring the area 3b/1 regions activated by vibrotactile stimulation of the contralateral radial interdigital pad. 4. The intrinsic signal evoked in area 3a by a series of heating stimuli to the contralateral radial interdigital pad (applied with a stationary probe/thermode) increased progressively in magnitude with repeated stimulation (exhibited slow temporal summation) and remained above prestimulus levels for a prolonged period after termination of repetitive stimulation. 5. Brief mechanical stimuli ("taps") applied to the contralateral radial interdigital pad with a probe/thermode maintained either at 37 degrees C or at 52 degrees C were accompanied by the development of an intrinsic signal in both area 3a and areas 3b/1. For the 52 degrees C stimulus, the area 3a intrinsic signal was larger and the intrinsic signal in areas 3b/1 smaller than the corresponding signals evoked by the 37 degrees C stimulus. 6. Spike discharge activity was recorded from area 3a neurons during a repetitive heating stimulus applied with a stationary probe/ thermode to the contralateral radial interdigital pad. Like the area 3a intrinsic signal elicited by repetitive heating of the same skin site, the area 3a neuron spike discharge activity also exhibited slow temporal summation and poststimulus response persistence. 7. The experimental findings suggest 1) a leading role for area 3a in the anterior parietal cortical processing of skin-heating stimuli, and 2) the presence of inhibitory interactions between the anterior parietal responses to painful and vibrotactile stimuli consistent with those demonstrated in recent cortical imaging and psychophysical studies of human subjects.

[1]  Nikolaus M. Szeverenyi,et al.  Persistent pain inhibits contralateral somatosensory cortical activity in humans , 1992, Neuroscience Letters.

[2]  R A Koeppe,et al.  Positron emission tomographic analysis of cerebral structures activated specifically by repetitive noxious heat stimuli. , 1994, Journal of neurophysiology.

[3]  Wolf Singer,et al.  Development and Plasticity of Cortical Processing Architectures , 1995, Science.

[4]  Karl J. Friston,et al.  Cortical and subcortical localization of response to pain in man using positron emission tomography , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[6]  A. Vania Apkarian,et al.  Spinothalamocortical inputs nonpreferentially innervate the superficial and deep cortical layers of SI , 1993, Neuroscience Letters.

[7]  Dan R. KenshaloJr.,et al.  The Role of the Cerebral Cortex in Pain Sensation , 1991 .

[8]  C. Gilbert,et al.  Synaptic physiology of horizontal connections in the cat's visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  E. G. Jones,et al.  Chemically distinct compartments of the thalamic VPM nucleus in monkeys relay principal and spinal trigeminal pathways to different layers of the somatosensory cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Mountcastle Vb,et al.  The cytoarchitecture of the postcentral gyrus of the monkey Macaca mulatta. , 1959 .

[11]  K. Kniffki Input to and Output from Lamina I Neurones in the Cat Spinal Cord , 1989 .

[12]  Karl J. Friston,et al.  Cerebral responses to pain in patients with atypical facial pain measured by positron emission tomography. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[13]  E. G. Jones,et al.  Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: distribution, laminar cortical projections, and relations to spinothalamic terminations , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Alan C. Evans,et al.  Distributed processing of pain and vibration by the human brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  V. Mountcastle,et al.  Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. , 1959, Bulletin of the Johns Hopkins Hospital.

[16]  A. Grinvald Real-time optical mapping of neuronal activity: from single growth cones to the intact mammalian brain. , 1985, Annual review of neuroscience.

[17]  A. Craig,et al.  Pain, temperature, and the sense of the body , 1996 .

[18]  A. Apkarian,et al.  Squirrel monkey lateral thalamus. I. Somatic nociresponsive neurons and their relation to spinothalamic terminals , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  R. Frostig,et al.  Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  H Burton,et al.  Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: Projections in the vicinity of the central sulcus , 1995, The Journal of comparative neurology.

[21]  Vania Apkarian Functional imaging of pain: new insights regarding the role of the cerebral cortex in human pain perception , 1995 .

[22]  S J Bolanowski,et al.  Heat-induced pain diminishes vibrotactile perception: a touch gate. , 1994, Somatosensory & motor research.

[23]  Andrew C. N. Chen,et al.  Somatosensory and frontal cortical processing during pain experience , 1996 .

[24]  M. Bushnell,et al.  A thalamic nucleus specific for pain and temperature sensation , 1994, Nature.

[25]  R. Dubner,et al.  Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses , 1977, Pain.

[26]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[27]  E. White Termination of Thalamic Afferents in the Cerebral Cortex , 1986 .

[28]  R. M. Siegel,et al.  High-resolution optical imaging of functional brain architecture in the awake monkey. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[29]  E. Rausell,et al.  Histochemical and immunocytochemical compartments of the thalamic VPM nucleus in monkeys and their relationship to the representational map , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  R. Porter,et al.  What is area 3a? , 1980, Brain Research Reviews.

[31]  T. Ebner,et al.  Use of voltage-sensitive dyes and optical recordings in the central nervous system , 1995, Progress in Neurobiology.

[32]  E G Jones,et al.  Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  E G Jones,et al.  Extent of intracortical arborization of thalamocortical axons as a determinant of representational plasticity in monkey somatic sensory cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.