Corticostriatal cells in comparison with pyramidal tract neurons: contrasting properties in the behaving monkey

Abstract

Antidromically identified neurons projecting to the putamen (CPNs) and pyramidal tract neurons (PTNs) were recorded from motor and premotor cortex of a monkey which performed a load-bearing task with the wrist. CPNs appeared as a uniform population with very slowly conducting axons and low spontaneous activity. In contrast to PTNs, they exhibited weak, mostly insignificant correlation with graded steady-state forces, responded to torque perturbations with remarkably long latency, and seemed to discharge much later with active movement. Collateral branching of PTNs to the putamen was found to be infrequent (1%). We suggest that the putamen receives a cortical message that is strikingly different from that sent down the pyramidal tract.The role of the putamen as part of a 'motor' circuit linking the basal ganglia with the neocortex has been evidenced by the demonstration of somatotopically well-organized projections from the sensory and motor cortices s'L°'12 and by recent findings on the relationship of single cells to specific aspects of motor behavior ~-3'1~ in the primate putamen. However, the functional significance of the corticostriatal part of this 'motor loop' remains obscure, mainly because the actual projection neurons to the putamen have until now not been neurophysiologically identified and studied in any animal preparation. Recent anatomical work stresses the independence of the cells of origin of the various corticofugal systems 9, thus possibly indicating their functional specialization. Although still a matter of controversy 4"5, collateral branching to the striatum of other descending fibers, namely of the pyramidal tract, seems to be negligible in the monkey s."> . Other, more general questions posed by our study relate (1) to the issue of columnar organization of the motor cortex, i.e. do neighboring clusters of different types of efferent cell in cortical layer V constitute a common module9"16?, and (2) do similarities within a particular corticofugal system transcend areaspecific differencesT? We have therefore compared the properties of antidromically identified corticoputamenal neurons (CPNs) and pyramidal tract neurons (PTNs) recorded from the primary motor cortex (MI) and postarcuate premotor area (PMA) in the behaving monkey.A fully trained, male rhesus monkey (8.5 kg) was used for the experiments. Under Nembutal anesthesia and after craniotomy over the left MI-hand-arm region, a recording cylinder (i.d. 18 mm) was installed and tilted in the vertical plane, so as to allow transdural microelectrode penetrations perpendicular to the cortical surface. Stereotaxic procedures were aided by the use of X-rays and NMR-tomography. A pair of teflon-insulated stainless steel wires of 150 /xm diameter (tips exposed over 200/~m and vertically separated by 2.5 mm) attached to a guide shaft was implanted within the left pyramidal tract (PT) at the most caudal level of the inferior olive. Another, similar bipolar stimulating electrode aimed at the left putamen was inserted

Recurrent Connection Patterns of Corticostriatal Pyramidal Cells in Frontal Cortex

“…A second subtype of CCS cell identified in rats projects to the brainstem (Donoghue and Kitai, 1981;Cowan and Wilson, 1994;Lévesque et al, 1996a). Although it remains to be investigated how often collaterals are issued from axons descending to the brainstem in the primate (Bauswein et al, 1989), in the rat frontal cortex, brainstem-projecting layer V neurons also frequently innervate the ipsilateral striatum (Lévesque et al, 1996a;Lévesque and Parent, 1998). In this study, we confirmed that CCS and CPn cells are mutually exclusive groups using doublefluorescence markers.…”

A Physiologically Plausible Model of Action Selection and Oscillatory Activity in the Basal Ganglia

“…The calibration process consisted of varying the I spon currents in each of STN, GP, and SNr while applying background cortical input consisting of low-frequency, unpatterned (Poisson series) spikes with a mean firing rate of f ϭ 3 spikes/s (Bauswein et al, 1989). Such a low rate is insufficient to cause reliable firing in striatum, consistent with numerous striatal recordings (Mahon et al, 2001(Mahon et al, , 2003.…”

Deep Brain Stimulation for Movement Disorders of Basal Ganglia Origin: Restoring Function or Functionality?

“…Combined single-cell/behavioral studies in primates have found highly specific changes in neuronal activity in relation to (trained) limb movements throughout the nodes of the motor circuit, particularly in relation to movement amplitude/velocity, However, the observed changes in discharge lag behind activity changes in the MC [42][43][44][45], and the activation of (antidromically identified) corticoputaminal neurons lags that of nearby corticofugal projections to brainstem and spinal cord [46,47]. Moreover, lesions interrupting the output of the motor circuit in the sensorimotor territory of GPi in normal primates and individuals with PD or dystonia [48], following pallidotomy, have little or no effect on reaction times, although a slowing of movement is a consistent finding [49][50][51][52].…”