Area 3a: topographic organization and cortical connections in marmoset monkeys.

The functional organization of area 3a, a cortical field proposed to be involved in somato-motor-vestibular integration, has never been described for any primate. In the present investigation, the topographic organization and connections of area 3a were examined in marmosets using electrophysiological recording and anatomical tracing techniques. Multi-unit neuronal activity was recorded at a number of closely spaced sites; receptive fields (RFs) for neurons were determined, and the optimal stimulus was identified. In all cases, neurons in area 3a responded to the stimulation of deep receptors on the contralateral body. The representation of the body in area 3a was from the toes and foot, to the hindlimb, trunk, forelimb, hand and face in a mediolateral progression. In all cases electrophysiological results were related to myeloarchitecture, and the map in area 3a was found to be coextensive with a strip of lightly to moderately myelinated cortex just rostral to the darkly myelinated 3b. To examine the cortical connections of area 3a, injections of anatomical tracers were made into electrophysiologically identified body part representations. Area 3a has dense intrinsic connections and receives substantial inputs from the primary motor cortex (M1), the supplementary motor area (SMA), areas 1 and 2, the second somatosensory area (S2), and areas in posterior parietal cortex (PP). The connections of area 3a indicate that integration of cortical representations of body parts occurs both within area 3a and between area 3a and other somatosensory and motor areas. In addition, there are differential patterns of interconnections between behaviorally relevant body part representations of area 3a, such as the forelimb, compared to other body part representations (hindlimb/ trunk), especially with 'higher order' cortical fields. This suggests that 3a may be an important component in a network that generates a common frame of reference for hand and eye coordinated reaching tasks.

[1]  J. Kaas,et al.  Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys , 1987, The Journal of comparative neurology.

[2]  H Asanuma,et al.  Activities of neurons in area 3a of the cerebral cortex during voluntary movements in the monkey. , 1974, Brain research.

[3]  J Tanji,et al.  Comparison of movement-related activity in two cortical motor areas of primates. , 1982, Journal of neurophysiology.

[4]  O. Grüsser,et al.  Corticofugal projections to the vestibular nuclei in squirrel monkeys: Further evidence of multiple cortical vestibular fields , 1993, The Journal of comparative neurology.

[5]  B L Whitsel,et al.  Anterior parietal cortical response to tactile and skin-heating stimuli applied to the same skin site. , 1996, Journal of neurophysiology.

[6]  S. Landgren,et al.  The projection of group I muscle afferents from the hindlimb to the contralateral thalamus of the cat. , 1970, Acta physiologica Scandinavica.

[7]  M. Merzenich,et al.  Frequency representation in auditory cortex of the common marmoset (Callithrix jacchus jacchus) , 1986, The Journal of comparative neurology.

[8]  J. Kaas The Segregation of Function in the Nervous System , 1995 .

[9]  S. Wise,et al.  Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.

[11]  L A Krubitzer,et al.  The dorsomedial visual area of owl monkeys: Connections, myeloarchitecture, and homologies in other primates , 1993, The Journal of comparative neurology.

[12]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[13]  C. Gilbert,et al.  Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  C. Avendaño,et al.  Area 3a in the cat. I. A reevaluation of its location and architecture on the basis of Nissl, myelin, acetylcholinesterase, and cytochrome oxidase staining , 1992, The Journal of comparative neurology.

[15]  L. L. Porter,et al.  Patterns of connectivity in the cat sensory‐motor cortex: A light and electron microscope analysis of the projection arising from area 3a , 1991, The Journal of comparative neurology.

[16]  G. Recanzone,et al.  Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. , 1992, Journal of neurophysiology.

[17]  O J Grüsser,et al.  Thalamic connections of the vestibular cortical fields in the squirrel monkey (Saimiri sciureus) , 1992, The Journal of comparative neurology.

[18]  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.

[19]  C. G. Phillips,et al.  Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex. , 1971, The Journal of physiology.

[20]  L A Krubitzer,et al.  Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns , 1990, Visual Neuroscience.

[21]  S. Landgren,et al.  Projection to cerebral cortex of Group I muscle afferents from the cat's hind limb , 1969, The Journal of physiology.

[22]  T. Pons,et al.  Primary motor cortex receives input from area 3a in macaques , 1990, Brain Research.

[23]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[24]  J. Kaas,et al.  Architectionis, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys , 1993, The Journal of comparative neurology.

[25]  R. Andersen,et al.  Change in motor plan, without a change in the spatial locus of attention, modulates activity in posterior parietal cortex. , 1998, Journal of neurophysiology.

[26]  J. B. Preston,et al.  Two representations of the hand in area 4 of a primate. I. Motor output organization. , 1982, Journal of neurophysiology.

[27]  J. Kaas,et al.  Cortical connections of the dorsomedial visual area in new world owl monkeys (Aotus trivirgatus) and squirrel monkeys (Saimiri sciureus) , 1998, The Journal of comparative neurology.

[28]  J. Kaas The reorganization of sensory and motor maps after injury in adult mammals , 2000 .

[29]  V. Mountcastle The visual functions of the parietal lobe , 1984, Behavioural Brain Research.

[30]  M. Merzenich,et al.  Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  J. Kaas,et al.  Movement representation in the dorsal and ventral premotor areas of owl monkeys: A microstimulation study , 1996, The Journal of comparative neurology.

[32]  L A Krubitzer,et al.  The somatosensory thalamus of monkeys: Cortical connections and a redefinition of nuclei in marmosets , 1992, The Journal of comparative neurology.

[33]  C. G. Phillips,et al.  Inputs from low threshold muscle and cutaneous afferents of hand and forearm to areas 3a and 3b of baboon's cerebral cortex. , 1976, The Journal of physiology.

[34]  J. Kaas,et al.  Connections of primary auditory cortex in the new world monkey, Saguinus , 1989, The Journal of comparative neurology.

[35]  J. Kleim,et al.  Functional reorganization of the rat motor cortex following motor skill learning. , 1998, Journal of neurophysiology.

[36]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  Lindsay Aitkin,et al.  Audition and the auditory pathway of a vocal new world primate, the common marmoset , 1993, Progress in Neurobiology.

[38]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[39]  D J Felleman,et al.  Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: possible relationships to sensory recovery in humans , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  B. Rockstroh,et al.  Increased Cortical Representation of the Fingers of the Left Hand in String Players , 1995, Science.

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

[42]  G. Recanzone,et al.  Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. , 1992, Journal of neurophysiology.

[43]  Leah Krubitzer,et al.  Interhemispheric connections of somatosensory cortex in the flying fox , 1998, The Journal of comparative neurology.

[44]  C. Darian‐Smith,et al.  Ipsilateral cortical projections to areas 3a, 3b, and 4 in the macaque monkey , 1993, The Journal of comparative neurology.

[45]  G. Elston,et al.  The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity , 1997, The Journal of comparative neurology.

[46]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[47]  M. Calford,et al.  The capacity for reorganization in adult somatosensory cortex , 1990 .

[48]  C. Darian‐Smith,et al.  MANUAL DEXTERITY: HOW DOES THE CEREBRAL CORTEX CONTRIBUTE? , 1996, Clinical and experimental pharmacology & physiology.

[49]  Jun Tanji,et al.  Activity of neurons in cortical area 3a during maintenance of steady postures by the monkey , 1975, Brain Research.

[50]  S P Wise,et al.  Submodality distribution in sensorimotor cortex of the unanesthetized monkey. , 1981, Journal of neurophysiology.

[51]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[52]  O. Grüsser,et al.  Cortico‐cortical connections and cytoarchitectonics of the primate vestibular cortex: A study in squirrel monkeys (Saimiri sciureus) , 1992, The Journal of comparative neurology.

[53]  M. Merzenich,et al.  Repetitive microstimulation alters the cortical representation of movements in adult rats. , 1990, Somatosensory & motor research.

[54]  R. Lane,et al.  Neural Correlates of Levels of Emotional Awareness: Evidence of an Interaction between Emotion and Attention in the Anterior Cingulate Cortex , 1998, Journal of Cognitive Neuroscience.

[55]  J. Kaas,et al.  Studies on the evolution of multiple somatosensory representations in primates: The organization of anterior parietal cortex in the new world callitrichid, Saguinus , 1986, The Journal of comparative neurology.

[56]  W M Jenkins,et al.  Frequency discrimination training engaging a restricted skin surface results in an emergence of a cutaneous response zone in cortical area 3a. , 1992, Journal of neurophysiology.

[57]  M G Rosa,et al.  Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus) , 1996, The Journal of comparative neurology.

[58]  B. Hyland,et al.  Comparison of neural activity in the supplementary motor area and in the primary motor cortex in monkeys. , 1991, Somatosensory & motor research.

[59]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[60]  D. Irvine,et al.  Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex , 1993, The Journal of comparative neurology.

[61]  J. B. Preston,et al.  Responses of cortical neurons (areas 3a and 4) to ramp stretch of hindlimb muscles in the baboon. , 1976, Journal of neurophysiology.

[62]  L A Krubitzer,et al.  The organization and connections of somatosensory cortex in marmosets , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  M. Wiesendanger,et al.  Ascending pathway of low-threshold muscle afferents to the cerebral cortex and its possible role in motor control. , 1982, Physiological reviews.

[64]  M Wiesendanger,et al.  Responses of neurones in motor cortex and in area 3A to controlled stretches of forelimb muscles in cebus monkeys. , 1975, The Journal of physiology.

[65]  Estrella Rausell,et al.  Area 3a in the cat II. Projections to the motor cortex and their relations to other corticocortical connections , 1992, The Journal of comparative neurology.

[66]  D. J. Felleman,et al.  Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation , 1983, Neuroscience.

[67]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[68]  O. Oscarsson,et al.  Short‐latency projections to the cat cerebral cortex from skin and muscle afferents in the contralateral forelimb , 1966, The Journal of physiology.

[69]  M G Rosa,et al.  Monocular focal retinal lesions induce short–term topographic plasticity in adult cat visual cortex , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[70]  L. Aitkin,et al.  Connections of the primary auditory cortex in the common marmoset, Callithrix jacchus jacchus , 1988, The Journal of comparative neurology.

[71]  E. G. Jones,et al.  Relationship of intrinsic connections to forelimb movement representations in monkey motor cortex: a correlative anatomic and physiological study. , 1991, Journal of neurophysiology.

[72]  J. Kaas,et al.  The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys , 1986, The Journal of comparative neurology.

[73]  J. Allman,et al.  Organization of the face representation in macaque motor cortex , 1980, The Journal of comparative neurology.

[74]  S P Wise,et al.  Neuronal responses in sensorimotor cortex to ramp displacements and maintained positions imposed on hindlimb of the unanesthetized monkey. , 1981, Journal of neurophysiology.

[75]  L. Krubitzer The organization of lateral somatosensory cortex in primates and other mammals , 1996 .