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Cortical mapping and laminar analysis of the cutaneous and proprioceptive inputs from the rat foreleg: an extra- and intra-cellular study

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The foreleg proprioceptive and cutaneous representations, in the Sm cortex of urethane-anesthetized rats was studied. Natural or electrical stimulations and stretches of single forearm muscles were used. Multiunitary, unitary or intra-cellular recordings were performed in the contra-lateral Sm cortex. The aims of the study were: 1 — to compare the proprioceptive and cutaneous maps 2 — to analyse the characteristics of the unitary responses and 3 — to study the laminar distribution of cutaneous and muscular inputs. It is shown that: 1 — the proprioceptive and cutaneous representations overlapped, except in the anterior part where only proprioceptive (mainly articular) responses were obtained. The representation of each stretched muscle extended over the whole cutaneous area, showing a total overlap between inputs from these muscles. 2–46% of the intracellularly recorded cells (n=215) responded to peripheral stimulation, and 30.7% were influenced by (at least) muscle stretch. The majority of excited cells showed cross-modal covergence, and among neurons responding to muscle stretch, 60% received inputs from the two muscles stretched. Two categories of EPSPs were found, and four neurons responded to cutaneous or muscular stimulation with a burst. 19% of the responding cells were inhibited by peripheral — mainly cutaneous — stimulations. 3 —Excited neurons were recorded in all layers, with just over half located in layer IV, whereas IPSPs were obtained mainly in layer V. The cells excited by cutaneous and muscular inputs (convergent neurons) were preponderant in layers IV to VI. This work shows that the cutaneous and muscular inputs reach the same area in Sm cortex, and that a majority of excited cells are “convergent”. The results are not in favor of an area 3a (by analogy with cats and monkeys) in the rat.

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References

  • Angel A, Banks D (1983) The functional organization of the forepaw sensorimotor cortex in the adult rat. J Physiol (Lond) 343: 62–82

    Google Scholar 

  • Chapin JK, Lin CS (1984) Mapping the body representation in the SI cortex of anesthetized and awake rats. J Comp Neurol 229: 199–213

    Google Scholar 

  • Chapin JK, Woodward DJ (1982) Cortico-cortical connections between physiologically and histologically defined zones in the rat SI and MI cortices. Abstr Soc Neurosci 8: 853A

  • Colonnier M (1981) The electron-microscopic analysis of the neuronal organization of the cerebral cortex. In: Schmitt FO, Worden FG, Adelman G, Dennis SG (eds) The organization of the cerebral cortex. MIT Press, Cambridge, pp 125–152

    Google Scholar 

  • Connors BW (1984) Initiation of synchronized neuronal bursting in neocortex. Nature 310: 685–687

    Google Scholar 

  • Connors BW, Gutnick MJ, Prince DA (1982) Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48: 1302–1320

    Google Scholar 

  • Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212: 76–88

    Google Scholar 

  • Dykes RW (1983) Parallel processing of somatosensory information: a theory. Brain Res Rev 6: 47–115

    Google Scholar 

  • Felleman DJ, Wall JT, Cusick CG, Kaas JH (1983) The representation of the body surface in SI of cats. J Neurosci 3: 1648–1669

    Google Scholar 

  • Gioanni Y, Lamarche M (1985) A reappraisal of rat motor cortex organization by intracortical microstimulation. Brain Res 344: 49–61

    Google Scholar 

  • Greene EC (1968) Anatomy of the rat. Hafner, New York

    Google Scholar 

  • Gutnick MJ, Connors BW, Prince DA (1982) Mechanisms of neocortical epileptogenesis in vitro. J Neurophysiol 45: 1321–1335

    Google Scholar 

  • Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66: 23–38

    Google Scholar 

  • Heath CJ, Hore J, Phillips CG (1976) Inputs from low threshold muscle and cutaneous afferents of hand and forearm to areas 3a and 3b of baboon's cerebral cortex. J Physiol (Lond) 257: 199–227

    Google Scholar 

  • Hersch SM, White EL (1981) Thalamocortical synapses involving identified neurons in mouse primary somato-sensory cortex: a terminal degeneration and Golgi/EM study. J Comp Neurol 195: 253–264

    Google Scholar 

  • Hummelsheim H, Wiesendanger M (1985) Is the hindlimb representation of the rat's cortex a “sensorimotor amalgam”? Brain Res 346: 75–81

    Google Scholar 

  • Hyvärinen J, Poranen A (1978) Receptive field integration and submodality convergence in the hand area of post-central gyrus of the alert monkey. J Physiol (Lond) 283: 539–556

    Google Scholar 

  • Iwamura Y, Tanaka M, Sakamoto M, Hikosaka O (1983a) Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey. Exp Brain Res 51: 315–326

    Google Scholar 

  • Iwamura Y, Tanaka M, Sakamoto M, Hikosaka O (1983b) Converging patterns of finger representation and complex response properties of neurons in area 1 of the first somatosensory cortex of the conscious monkey. Exp Brain Res 51: 327–337

    Google Scholar 

  • Jones EG, Porter R (1980) What is area 3a? Brain Res Rev 2: 1–43

    Google Scholar 

  • Kang R, Herman D, Zarzecki P (1985) Convergence of sensory inputs in somatosensory cortex: interactions from separate afferent sources. Exp Brain Res 57: 271–278

    Google Scholar 

  • Lamour Y, Jobert A (1982) Laminar distribution and convergence of deep and superficial peripheral inputs in the forelimb representation of rat SI somatosensory cortex. J Physiol (Paris) 78: 158–162

    Google Scholar 

  • Landgren S, Silfvenius H (1969) Projection to cerebral cortex of group I muscle afferents from the cat's hindlimb. J Physiol (Lond) 200: 353–372

    Google Scholar 

  • Landry P, Deschenes M (1981) Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat. J Comp Neurol 199: 345–372

    Google Scholar 

  • Lipski J (1981) Antidromic activation of neurons as an analytic tool in the study of the central nervous system. J Neurosci Methods 4: 1–32

    Google Scholar 

  • Lucier GE, Ruegg DJ, Wiesendanger M (1975) Responses of neurones in motor cortex and in area 3a to controlled stretches of forelimb muscles in cebus monkeys. J Physiol (Lond) 251: 833–853

    Google Scholar 

  • McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782–806

    Google Scholar 

  • Merzenich MM, Kaas JH, Sur M, Lin CS (1978) Double representation of the body surface within cytoarchitectonic areas 3b and 1 in “SI” in the owl monkey (Aotus trivirgatus). J Comp Neurol 181: 41–74

    Google Scholar 

  • Mountcastle VB, Powell TPS (1959) Neural mechanisms subserving cutaneous sensibility, with special reference to the role of afferent inhibition in sensory perception and discrimination. Bull Johns Hopkins 105: 201–232

    Google Scholar 

  • Neafsey EJ, Bold EL, Haas G, Hurley-Gius KM, Quirk G, Sievert CF, Terreberry RR (1986) The organization of the rat motor cortex: a microstimulation mapping study. Brain Res Rev 11: 77–96

    Google Scholar 

  • Oscarsson O, Rosen I (1963) Projection to cerebral cortex of large muscle spindle afferents in forelimb nerves of the cat. J Physiol (Lond) 169: 924–945

    Google Scholar 

  • Oscarsson O, Rosen I, Sulg I (1966) Organization of neurones in the cat cerebral cortex that are influenced from group I muscle afferents. J Physiol (Lond) 183: 189–210

    Google Scholar 

  • Phillips CG, Powell TPS, Wiesendanger M (1971) Projection from low muscle afferents of hand and forearm to area 3a of baboon's cortex. J Physiol (Lond) 217: 419–446

    Google Scholar 

  • Rosen I, Asanuma H (1973) Natural stimulation of group I activated cells in the cerebral cortex of the awake cat. Exp Brain Res 16: 247–254

    Google Scholar 

  • Sanderson KJ, Welker W, Shambes GM (1984) Reevaluation of motor cortex and sensorimotor overlap in cerebral cortex of albino rats. Brain Res 292: 251–260

    Google Scholar 

  • Swett JE, Bourassa CM (1966) Short latency activation of pyramidal tract cells by group I afferent volleys in the cat. J Physiol (Lond) 189: 101–117

    Google Scholar 

  • Waite PME (1973a) Somatotopic organization of vibrissal responses in the ventro-basal complex of the rat thalamus. J Physiol (Lond) 228: 527–540

    Google Scholar 

  • Waite PME (1973b) The responses of the cells in the rat thalamus to mechanical movements of the whiskers. J Physiol (Lond) 228: 541–561

    Google Scholar 

  • Welker C (1971) Microelectrode delineation of fine grain somatotopic organization of SmI cerebral neocortex in albino rat. Brain Res 26: 259–275

    Google Scholar 

  • Welker W, Sanderson KJ, Shambes GM (1984) Patterns of afferent projections to transitional zones in the somatic sensorimotor cerebral cortex of albino rats. Brain Res 292: 261–267

    Google Scholar 

  • White EL (1978) Identified neurons in mouse SmI cortex which are postsynaptic to thalamocortical axon terminals: a combined Golgi-electron microscopic and degeneration study. J Comp Neurol 181: 627–662

    Google Scholar 

  • White EL (1979) Thalamocortical synaptic relations. A review with emphasis on the projections of specific thalamic nuclei to the primary sensory areas of the neocortex Brain Res Rev 1: 275–311

    Google Scholar 

  • Woolsey CN (1958) Organization of somatic sensoy and motor areas of the cerebral cortex. In: Harlow H, Woolsey CN (eds) Biological and biochemical bases of behavior. University Wisconsin Press, Madison, pp 63–81

    Google Scholar 

  • Zarzecki P, Wiggin DM (1982) Convergence of sensory inputs upon projection neurons of somatosensory cortex. Exp Brain Res 48: 28–42

    Google Scholar 

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Gioanni, Y. Cortical mapping and laminar analysis of the cutaneous and proprioceptive inputs from the rat foreleg: an extra- and intra-cellular study. Exp Brain Res 67, 510–522 (1987). https://doi.org/10.1007/BF00247284

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  • DOI: https://doi.org/10.1007/BF00247284

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