Precise location of fast and slow pyramidal tract cells in cat sensorimotor cortex

Naito, Haruhiko; Nakamura, Kyugo; Kurosaki, Takanori; Tamura, Yukiko

doi:10.1016/0006-8993(69)90047-x

Cited by 33 publications

(6 citation statements)

References 7 publications

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“…cells monosynaptically (Amassian & Weiner 1966;Asanuma & Okada 1962) and p.t. neurons have been shown by dye injection to be pyramidal cells (Naito, Nakamura, Kurosaki & Tamura 1969). Thus there is good agreement between the anatomical and physiological findings with respect to the major site of termination of afferents to the motor cortex and in addition the correlation between the asymmetric membrane special izations and the excitatory action of the afferents confirms the correlation between structure and function made in the cerebellum (Uchizono 1965) and elsewhere (Gray 1969).…”

Section: Synthesissupporting

confidence: 62%

An experimental electron microscopy study of afferent connections to the primate motor and somatic sensory cortices

Sloper

Powell

1979

Phil. Trans. R. Soc. Lond. B

124

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An experimental electron microscope (e.m.) study has been made of the termination of the afferent connections to the primate sensori-motor cortex. Following large, stereotaxically placed thalamic lesions, degeneration in the motor and somatic sensory cortices was studied at survival periods of 4 and 5 days. Degenerating thalamocortical terminals had asymmetric membrane specializations. In the motor cortex 89.5% made synapses on to dendritic spines, 9% on to dendritic shafts and 1.5% on to cell somata; in the somatic sensory area 89% made synapses on to spines, 11 % on to dendritic shafts and one example contacted a cell soma and a spine. A considerable number of the spines receiving synapses from degenerating thalamo-cortical terminals were traced to their parent dendrites and these were of the pyramidal type whereas the dendritic shafts and cell somata contacted by degenerating thalamo-cortical terminals were mostly of the large stellate type. Most of the thalamo-cortical degeneration in both cortical areas occurred in a dense band in the upper two thirds of layer IV and the lower half of layer III but a number of degenerating terminals were found deep to this; in the motor cortex a second, less dense, band of degeneration was present in the lower part of layer V and top of layer VI. Degenerating thalamo-cortical terminals making synapses on to dendritic shafts and cell somata were scattered through the deep half of the cortex and not concentrated in the dense band of degeneration and so formed a greater proportion of the degeneration in the deep layers, particularly in the motor cortex. Sections cut parallel to the pial surface in layer IV of the motor cortex showed a statistically significant association between the degenerating thalamocortical axon terminals and the bundles of apical dendrites present at this level. Degeneration of commissural fibres was studied after removal of the contralateral sensori-motor cortex. Degenerating terminals had asymmetric membrane specializations. In the motor cortex 96% made synapses on to dendritic spines, 3% contacted dendritic shafts and one example made an axosomatic synapse; in area 3 97% made synapses on to dendritic spines and 3% contacted dendritic shafts. A number of the spines receiving synapses from degenerating commissural axon terminals were traced to their parent dendrites and these were of the pyramidal type. The cell soma and the majority of the dendritic shafts receiving synapses from commissural terminals were of the large stellate type although some of the dendritic shafts were probably those of small stellate cells. In the motor cortex degenerating commissural axon terminals were found in all cortical layers but were relatively more dense in layer I, the upper part of layer III, the upper part of layer V and the lowest part of layer V with layer V I; in the somatic sensory cortex most degenerating commissural terminals were found in the superficial half of the cortex. Following lesions of the primary somatic sensory cortex (SI) or of area 6 of the premotor cortex, degenerating terminals making asymmetric synapses were found in the motor cortex. Of the terminals of association fibres from SI, 82% made synapses on to dendritic spines and 18% on to dendritic shafts; of those fibres from area 6, 76% made synapses on to dendritic spines and 24% on to dendritic shafts. For both these association fibre connections, a proportion of the dendritic shafts contacted were clearly identifiable as those of large stellate cells. Terminals of both association connections occurred in all cortical layers with no obvious concentrations at any particular depth.

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Section: Synthesissupporting

confidence: 62%

An experimental electron microscopy study of afferent connections to the primate motor and somatic sensory cortices

Sloper

Powell

1979

Phil. Trans. R. Soc. Lond. B

124

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“…For example, faster APs could limit calcium influx during prolonged AP trains, reducing activation of potassium channels responsible for spike-frequency adaptation and thus favoring a more regular firing pattern; this in turn could facilitate rate-coded output to the spinal cord. That fast somatic APs are indeed associated with fast axonal APs is indicated by the correlation between somatically recorded AP width and axonal conduction velocity for pyramidal tract-type projection neurons in cat and primate cortex (Stefanis and Jasper 1964;Takahashi 1965;Naito et al 1969;Calvin and Sypert 1976;Deschenes et al 1979;Murray and Coulter 1981;Sakai and Woody 1988;Baranyi et al 1993;Rathelot and Strick 2006;Vigneswaran et al 2011).…”

Section: Discussionmentioning

confidence: 98%

“…Corticospinal soma size was not associated with AP waveform variability. In other species, certain electrophysiological properties, such as axonal conduction velocity (Naito et al 1969;Deschenes et al 1979) and repetitive firing pattern (Tseng and Prince 1993), do correlate with somatic size. The restricted range of soma sizes observed here for mouse corticospinal neurons may have been a factor.…”

Section: Discussionmentioning

confidence: 99%

Intrinsic Electrophysiology of Mouse Corticospinal Neurons: a Class-Specific Triad of Spike-Related Properties

2012

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Corticospinal pyramidal neurons mediate diverse aspects of motor behavior. We measured spike-related electrophysiological properties of identified corticospinal neurons in primary motor cortex slices from young adult mice. Several consistent features were observed in the suprathreshold responses to current steps: 1) Corticospinal neurons fired relatively fast action potentials (APs; width at half-maximum 0.65 ± 0.13 ms, mean ± standard deviation [SD]) compared with neighboring callosally projecting corticostriatal neurons. Corticospinal AP width was intermediate between 2 classes of inhibitory interneuron in layer 5B. Spike-to-spike variability in AP width and other spike waveform parameters was low, even during repetitive firing up to 20 Hz, that is, the relative narrowness of corticospinal APs was essentially frequency independent. 2) Frequency-current (f-I) relationships were nearly linear. 3) Trains of APs displayed regular firing, with rates typically staying constant or accelerating over time. Corticospinal neurons recorded from older mice (up to 4 months) or from a separate lateral cortical area (Region B; corresponding to secondary somatosensory cortex) showed generally similar intrinsic properties. Our findings have implications for interpreting spike waveforms of in vivo recorded neurons in the motor cortex. This analysis provides a framework for further biophysical and computational investigations of corticospinal neurons and their roles in motor cortical function.

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“…Neurons with fast-conducting axons generally have larger cell bodies than those with slow axons (Deschênes et al 1979; Naito et al 1969; Sakai and Woody 1988; Sloper and Powell 1979; Tomasi et al 2012), although the precise relationship between cell body and axon size is far from established. However, it is plausible that PTNs with thin axons may have small cell bodies and so be difficult to isolate in cortical recordings.…”

Section: Discussionmentioning

confidence: 99%

Axon diameters and conduction velocities in the macaque pyramidal tract

Firmin

Field

Maier

et al. 2014

Journal of Neurophysiology

116

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Small axons far outnumber larger fibers in the corticospinal tract, but the function of these small axons remains poorly understood. This is because they are difficult to identify, and therefore their physiology remains obscure. To assess the extent of the mismatch between anatomic and physiological measures, we compared conduction time and velocity in a large number of macaque corticospinal neurons with the distribution of axon diameters at the level of the medullary pyramid, using both light and electron microscopy. At the electron microscopic level, a total of 4,172 axons were sampled from 2 adult male macaque monkeys. We confirmed that there were virtually no unmyelinated fibers in the pyramidal tract. About 14% of pyramidal tract axons had a diameter smaller than 0.50 μm (including myelin sheath), most of these remaining undetected using light microscopy, and 52% were smaller than 1 μm. In the electrophysiological study, we determined the distribution of antidromic latencies of pyramidal tract neurons, recorded in primary motor cortex, ventral premotor cortex, and supplementary motor area and identified by pyramidal tract stimulation (799 pyramidal tract neurons, 7 adult awake macaques) or orthodromically from corticospinal axons recorded at the mid-cervical spinal level (192 axons, 5 adult anesthetized macaques). The distribution of antidromic and orthodromic latencies of corticospinal neurons was strongly biased toward those with large, fast-conducting axons. Axons smaller than 3 μm and with a conduction velocity below 18 m/s were grossly underrepresented in our electrophysiological recordings, and those below 1 μm (6 m/s) were probably not represented at all. The identity, location, and function of the majority of corticospinal neurons with small, slowly conducting axons remains unknown.

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Precise location of fast and slow pyramidal tract cells in cat sensorimotor cortex

Cited by 33 publications

References 7 publications

An experimental electron microscopy study of afferent connections to the primate motor and somatic sensory cortices

An experimental electron microscopy study of afferent connections to the primate motor and somatic sensory cortices

Intrinsic Electrophysiology of Mouse Corticospinal Neurons: a Class-Specific Triad of Spike-Related Properties

Axon diameters and conduction velocities in the macaque pyramidal tract

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