Morphology of pyramidal neurones in monkey motor cortex and the synaptic actions of their intracortical axon collaterals.

Abstract

Pyramidal neurones in the precentral motor area of the monkey were studied using intracellular techniques. Pyramidal tract neurones (PTNs) were identified by antidromic activation from the cerebral peduncles or medullary pyramids. Orthodromic responses were recorded in PTNs and in other pyramidal neurones when antidromic volleys were set up by stimulation of the peduncles or pyramids. The neurones were then labelled by intracellular ionophoresis of horseradish peroxidase and their morphology examined. All neurones studied were identified as pyramidal cells according to their morphology. Six pyramidal neurones located in lamina V were stained; they included two fast PTNs and two slow PTNs. The morphology of all pyramidal neurones in this lamina (fast PTNs, slow PTNs and those pyramidal cells that were not antidromically characterized) was essentially similar. A single apical dendrite branched as it ascended and its terminals arborized subpially. Numerous lateral and oblique dendrites branched from the apical dendrites in lamina V and near its border with lamina III: short basal dendrites arborized in the vicinity of the soma in lamina V. Long basal dendrites had a wider field of arborization in lamina V and sometimes extended into lamina VI. Three to five collaterals from the axon of lamina V cells in the cortex and arborized in laminae V and VI. Short collateral branches arborized in the vicinity of the soma in the region of the basal and lateral dendrites. Long collateral branches could be traced over long distances (often more than 1 mm). One pyramidal neurone in this lamina (a fast PTN) lacked short collateral branches from the axon. Four pyramidal neurones in lamina III were stained well. The dendritic morphology of all these neurones was similar. Apical dendrites branched as they ascended and terminated subpially. Lateral and basal dendrites formed a column of dendritic branches around the soma. No long basal dendrites were seen. The number and arborization of intracortical collaterals from the axon of lamina III cells varied widely; from three to twelve collaterals arose from the axon. The biggest arbor of collateral branches involved all the cortical laminae and was about 3 mm wide mediolaterally, while the smallest arbor was restricted mainly to lamina III in the vicinity of the soma. One neurone in this lamina also lacked short collateral branches from the axon. Antidromic volleys from the pyramidal tract evoked excitatory responses in fast PTNs, predominantly inhibitory responses in slow PTNs and either excitatory or inhibitory responses in other pyramidal neurones in lamina V. Antidromic volleys from the cerebral peduncles evoked mainly excitatory responses in all three types of neurones. EPSPs evoked by PTN recurrent collaterals were probably monosynaptic and were mediated by the axons of both fast and slow PTNs. IPSPs evoked by these collaterals were probably disynaptic and clearly involved axons of fast PTNs in some cases. Pyramidal neurones of lamina III were inhibited by the recurrent collaterals of PTNs when the axon collaterals were activated from the peduncles or the pyramids. PTNs interact through their intracortical collaterals with other PTNs and with other projection neurones in the cortex. Variations in the intracortical arborizations of these collaterals provide the substrate for variations in the potential for interactions among different individual neurones.