Abstract
The activity patterns of rhythmically firing neurons in monkey primary somatosensory cortex (SI) were studied during trained wrist movements that were performed in response to palmar vibration. Of 1,222 neurons extracellularly recorded in SI, 129 cells (∼11%) discharged rhythmically (at ∼30 Hz) during maintained wrist position. During the initiation of vibratory-cued movements, neuronal activity usually decreased at ∼25 ms after vibration onset followed by an additional decrease in activity at ∼60 ms prior to movement onset. Rhythmically firing neurons are not likely to be integrate-and-fire neurons because, during activity changes, their rhythmic firing pattern was disrupted rather than modulated. The activity pattern of rhythmically firing neurons was complimentary to that of quickly adapting SI neurons recorded during the performance of this task (Nelson et al., 1991). Moreover, disruptions of rhythmic activity of individual SI neurons were similar to those reported previously for local field potential (LFP) oscillations in sensorimotor cortex during trained movements (Sanes and Donoghue, 1993). However, rhythmic activity of SI neurons did not wax and wane like LFP oscillations (Murthy and Fetz, 1992; Sanes and Donoghue, 1993). It has been suggested that fast (20–50 Hz) cortical oscillations may be initiated by inhibitory interneurons (Cowan and Wilson, 1994; Llinas et al., 1991; Stern and Wilson, 1994). We suggest that rhythmically firing neurons may tonically inhibit quickly adapting neurons and release them from the inhibition at go-cue onsets and prior to voluntary movements. It is possible that rhythmically active neurons may evoke intermittent oscillations in other cortical neurons and thus regulate cortical population oscillations.
References
Ahissar E, Vaadia E (1990) Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis.Proc. Natl. Acad. Sci. USA 87:8935–8939.
Bouyer JJ, Montaron MF, Rougeul A (1981) Fast fronto-parietal rhythms during combined focused attentive behavior and immobility in cat: Cortical and thalamic localizations.Electroenceph. Clin. Neurophysiol 51:244–252.
Bouyer JJ, Montaron MF, Vahnee JM, Albert MP, Rougeul A (1987) Anatomical localization of cortical beta rhythms in cat.Neuroscience 22:863–869.
Brooks VB (1959) Contrast and stability in the nervous system.Trans. NY Acad. Sci. 21:387–394.
Burke D, Gandevia SC, Macefield G (1987) Responses to passive movements of receptors in joint, skin and muscle of the human hand.J. Physiol. (London) 402:347–361.
Chagnac-Amitai Y, Connors BW (1989) Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex.J. Neurophys. 62:1149–1162.
Chapin JK, Woodward DJ (1982) Somatic sensory transmission to the cortex during movement: gating of single cell responses to touch.Exp. Neurol. 78:654–669.
Chapman CE, Jiang W, Lamarre Y (1988) Modulation of lemniscal input during conditioned arm movements in the monkey.Exp. Brain Res. 72:316–334.
Cohen DAD, Prud'Homme MJL, Kalaska JF (1994) Tactile activity in primate primary somatosensory cortex during active arm movements: Correlation with receptive field properties.J. Neurophysiol. 71:161–172.
Colburn TR, Evarts EV (1978) Long-loop adjustments during intended movements: Use of brushless DC torque motors in studies of neuromuscular function. In: JE Desmedt, ed. Progress in Clinical Neurophysiology, Karger, New York, 4:153–166.
Coquery J-M (1978) Role of active movements in control of afferent input from skin in cat and man. In: G Gordon, ed. Active touch: The mechanisms of object manipulation: A multidisciplinary approach. Pergamon, Oxford, pp. 161–169.
Cowan RL, Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in rat medial agranular cortex.J. Neurophysiol. 71:17–31.
Dyhre-Poulsen P (1978) Perception of tactile stimuli before ballistic and during tracking movements. In: G Gordon, ed. Active touch: The mechanisms of object manipulation: A multidisciplinary approach. Pergamon, Oxford, pp. 171–176.
Dykes RW, Landry P, Metherate R, Hicks TP (1984) Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons.J. Neurophysiol. 52:1066–1093.
Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck HJ (1988) Coherent oscillations: A mechanism of feature linking in the visual cortex? Biol. Cybern. 60:121–130.
Ellaway PH (1977) An application of cumulative sum technique (cusums) to neurophysiology.J. Physiol. (Lond.) 265:1–2P.
Engel AK, König P, Kreiter AK, Schulen TB, Singer W (1992) Temporal coding in the visual cortex: New vistas on integration in the nervous system.Trends in Neurosci. 15:218–226.
Evarts EV (1966) Methods for recording activity of individual neurons in moving animals. In: RF Rushmer, ed. Methods in medical research. Yearbook, Chicago, 2:241–250.
Ghose GM, Freeman RD (1992) Oscillatory discharge in the visual system: Does it have a functional role?J. Neurophysiol. 68:1558–1574.
Gray CM (1994) Synchronous oscillations in neuronal systems: Mechanisms and functions.J. Comput. Neurosci. 1:11–38.
Gray CM, Engel AK, König P, Singer W (1991) Mechanisms underlying the generation of neuronal oscillations in cat visual cortex. In: E Basar, TH Bullock, eds. Induced rhythmicities in the brain. Birkhauser, Boston, pp. 29–45.
Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex.Proc. Natl. Acad. Sci. USA 86:1698–1702.
Hendry SHC, Jones EG, Emson PC, Lawson DEM, Heizmann CW, Streit P (1989) Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities.Exp. Brain Res. 76:467–472.
Horowitz P, Hill W (1980) The Art of Electronics. Cambridge Univ Press, Cambridge.
Istvan PJ, Zarzecki P (1994) Intrinsic discharge patterns and somatosensory inputs for neurons in racoon primary somatosensory cortex.J. Neurophysiol. 72:2827–2836.
Jagadeesh B, Gray CM, Ferster D (1992) Visually evoked oscillations of membrane potential in cells of cat visual cortex.Science 257:552–554.
Jiang W, Chapman CE, Lamarre Y (1991) Modulation of the cutaneous responsiveness of neurons in the primary somatosensory cortex during conditioned arm movements in the monkey.Exp. Brain Res. 84:342–354.
Jones EG (1975) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey.J. Comp. Neurol 160:205–268.
Jones EG (1986) Connectivity of the primate sensory-motor cortex. In: EG Jones, A Peters, eds. Cerebral Cortex. Sensory-Motor Areas and Aspects of Cortical Connectivity. Plenum Press, New York and London, 5:113–183.
Kawaguchi Y (1993) Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex.J. Neurophysiol. 69:416–431.
Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbuminD28k− immunoreactive neurons in layer V of rat frontal cortex.J. Neurophysiol. 70:387–395.
Lebedev MA, Denton JM, Nelson RJ (1994) Vibration-entrained and premovement activity in monkey primary somatosensory cortex.J. Neurophysiol. 72:1654–1673.
Lebedev MA, Nelson RJ (1993) Modulation of rhythmic firing of monkey primary somatosensory cortical (SI) and neostriatal (NS)' neurons during active hand movements. (319.8).Society for Neuwscience Abstracts 19:781.
Lemon R (1984) Methods for Neuronal Recording in Conscious Animals. IBRO handbook series:Methods in the Neurosciences Vol. 4. John Wiley & Sons, Chichester, UK.
Llinas RR (1990) Intrinsic electrical properties of nerve cells and their role in network oscillation.Cold Spring Harb Symp. on Quant. Biol. 55:933–938.
Llinas RR, Grace AA, Yarom Y (1991) In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10-to 50-Hz frequency range.Proc. Natl. Acad. Sci. USA 88:897–901.
Lopes da Silva F (1991) Neural mechanisms underlying brain waves: From neural membranes to networks.Electroenceph. Clin. Neurophysiol. 79:81–93.
Lytton WW, Sejnowski TJ (1991) Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons.J. Neurophysiol. 66:1059–1079.
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.
Mountcastle VB, Talbot WH, Sakata H, Hyvèrinen J (1969) Cortical neuronal mechanisms in flutter-vibration studies in unanesthetized monkeys: Neuronal periodicity and frequency discrimination.J. Neurophysiol. 32:452–484.
Mountcastle VB, Steinmetz MA, Romo R (1990) Frequency discrimination in the sense of flutter: Psychophysical measurements correlated with postcentral events in behaving monkeys.J. Neurosci. 10:3032–3044.
Murthy VN, Fetz EE (1992) Coherent 25-to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys.Proc. Natl. Acad. Sci. USA 89:5670–5674.
Murthy VN, Fetz EE (1994) Synchronization of primate sensorimotor cortex neurons during 20–40 Hz field potential oscillations. (403.16).Society for Neuroscience Abstracts 20:984.
Nelson RJ (1987) Activity of monkey primary somatosensory cortical neurons changes prior to active movement.Brain Res. 406:402–407.
Nelson RJ (1988) Set related and premovement related activity of primate somatosensory cortical neurons depends upon stimulus modality and subsequent movement.Brain Res. Bull. 21:411–424.
Nelson RJ, Smith BN, Douglas VD (1991) Relationship between sensory responsiveness and premovement activity of quickly adapting neurons in areas 3b and 1 of monkey primary somatosensory cortex.Exp. Brain Res. 84:75–90.
Nunñez A, Amzica F, Steriade M (1992) Voltage-dependent fast (20–40 Hz) oscillations in long-axoned neocortical neurons.Neuroscience 51:7–10.
Perkel DH, Gerstein G, Moore G (1967) Neuronal spike trains and stochastic point processes I. The single spike train.Biophys. J. 7:391–418.
Poggio T, Viernstein L (1964) Time series analysis of impulse sequences of thalamic somatic sensory neurons.J. Neurophysiol. 27:517–545.
Prochazka A (1985) Proprioception during movement.Can. J. Physiol. Pharmacol 64:499–504.
Ramón y Cajal S (1911)Histologie du Système Nerveux de l'Homme et des Vertébrés. Vol. 2. Maloine, Paris.
Rodieck RW, Kiang Ny-S, Gerstein GL (1962) Some quantitative methods for the study of spontaneous activity of single neurons.Biophys. J. 2:351–368.
Rougeul A, Bouer JJ, Dedet L, Debray O (1979) Fast somato-parietal rhythms during combined focal attention in baboon and squirrel monkey.Electroenceph. Clin. Neurophysiol. 46:310–319.
Rushton DN, Rothwell JC, Graggs MD (1981) Gating of somatosensory evoked potentials during different kinds of movement in man.Brain 104:465–491.
Sanes JN, Donoghue JP (1993) Oscillations in local field potentials of the primate motor cortex during voluntary movements.Proc. Natl. Acad. Sci. USA 90:4470–4474.
Segundo JP, Perkel DH, Wyman H, Hegstad H, Moore GP (1968) Input-output relations in computer-simulated nerve cells. Influence of the statistical properties, strength, number and interdependence of excitatory pre-synaptic terminals.Kibernetic 4:157–171.
Sheer DE (1989) Sensory and cognitive 40-Hz event-related potentials: Behavioral correlates, brain function, and clinical applications. In: E Basar, TH Bullock, eds.Springer Series in Brain Dynamics 2. Springer-Verlag, Berlin, Heidelberg, pp. 339–374.
Siebler M, Köller H, Rose G, Müller HW (1991) An improved graphical method for pattern recognition from spike trains of spontaneously active neurons.Exp. Brain Res. 90:141–146.
Silva LR, Amitai Y, Connors BW (1991) Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons.Science 251:432–435.
Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning.Annu. Rev. Physiol. 55:349–374.
Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs.J. Neurosci. 13:334–350.
Somogyi P, Cowey A (1981) Combined Golgi and electron microscopic study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey.J. Comp. Neurol. 195:547–566.
Soso MJ, Fetz EE (1980) Responses of identified cells in postcentral cortex of awake monkeys during comparable active and passive joint movements.J. Neurophysiol. 43:1090–1110.
Steriade M (1993) Central core modulation of spontaneous oscillations and sensory transmission in thalamocortical systems.Curr. Opin. Neurobiol. 3:619–625.
Stern EA, Wilson CJ (1994) High-frequency activity in the depolarized state of corticostriatal and striatal neurons. (238.12).Society for Neuroscience Abstracts 20:565.
Surmeier DJ, Towe AL (1987a) Properties of proprioceptive neurons in the cuneate nucleus of the cat.J. Neurophysiol. 57:938–961.
Surmeier DJ, Towe AL (1987b) Intrinsic features contributing to spike train patterning in proprioceptive cuneate neurons.J. Neurophysiol. 57:962–976.
Vaadia E, Kurata K, Wise, SP (1988) Neuronal activity preceding directional and nondirectional cues in the premotor cortex of rhesus monkeys.Somatosensory and Motor Research 6:207–230.
White EL (1989) Cortical Circuits: Synaptic Organization of the Cerebral Cortex: Structure, Function and Theory. Birkhäuser, Boston, MA.
Wiesendanger M, Miles TS (1982) Ascending pathway of lowthreshold muscle afférents to the cerebral cortex and its possible role in motor control.Physiol. Rev. 62:1234–1270.
Wilson CJ, Groves PM (1981) Spontaneous firing patterns of identified spiny neurons in the rat neostriatum.Brain Res. 220:67–80.
Wilson FAW, Scalaidhe SP, Goldman-Rakic PS (1994) Functional synegism between putative γ-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex.Proc. Natl. Acad. Sci. USA 91:4009–4013.
Wilson CJ, Young SJ, Groves PM (1977) Statistical properties of neuronal spike trains in the substantia nigra: Cell types and their interactions.Brain Res. 136:243–260.
Zadeh LA (1957) Signal-flow graphs and random signals.Proc. IRE 45:1413–1414.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lebedev, M.A., Nelson, R.J. Rhythmically firing (20–50 Hz) neurons in monkey primary somatosensory cortex: Activity patterns during initiation of vibratory-cued hand movements. J Comput Neurosci 2, 313–334 (1995). https://doi.org/10.1007/BF00961443
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00961443