SPONTANEOUS FIRING PATTERNS AND AXONAL PROJECTIONS OF SINGLE CORTICOSTRIATAL NEURONS IN THE RAT MEDIAL AGRANULAR CORTEX

1. Spontaneous fluctuations of membrane potential, patterns of spontaneous firing, dendritic branching patterns, and intracortical and striatal axonal arborizations were compared for two types of corticostriatal neurons in the medial agranular cortex of urethan-anesthetized rats: 1) pyramidal tract (PT) cells identified by antidromic activation from the medullary pyramid and 2) crossed corticostriatal (CST) neurons identified by antidromic activation from the contralateral neostriatum. The ipsilateral corticostriatal projections of intracellularly stained PT neurons as well as contralateral corticostriatal neurons were confirmed after labeling by intracellular injection of biocytin. 2. All well-stained PT neurons had intracortical and intrastriatal collaterals. The more common type (6 of 8) was a large, deep layer V neuron that had an extensive intracortical axon arborization but a limited axon arborization in the neostriatum. The less common type of PT neuron (2 of 8) was a medium-sized, superficial layer V neuron that had a limited intracortical axon arborization but a larger and more dense intrastriatal axonal arborization. Both subclasses of PT neurons had anatomic and physiological properties associated with slow PT cells in cats and monkeys and conduction velocities <10 m/s. All of the PT cells but one were regular spiking cells. The exceptional cell fired intrinsic bursts. 3. Intracellularly stained CST neurons were located in the superficial half of layer V and the deep part of layer III. Their layer I apical dendrites were few and sparsely branched. Their axons gave rise to an extensive arbor of local axon collaterals that distributed in the region of the parent neuron, frequently extending throughout the more superficial layers, including layer I. Axon collaterals were also traced to the corpus callosum, as expected from their contralateral projections, and they contributed axon collaterals to the ipsilateral neostriatum. In the neostriatum, these axons formed extended arborizations sparsely occupying a large volume of striatal tissue. All CST neurons were regular spiking cells. 4. Both types of cells displayed spontaneous membrane fluctuations consisting of a polarized state (-60 to -90 mV) that was interrupted by 0.1- to 3.0-s periods of depolarization ( -55 to -45 mV) accompanied by action potentials. The membrane potential was relatively constant in each state, and transitions between the depolarized and hyperpolarized states were sometimes periodic with a frequency of 0.3-1.5 Hz. A much faster (30-45 Hz) subthreshold oscillation of the membrane potential was observed only in the depolarized state and triggered action potentials that locked to the depolarizing peaks of this rhythm. The phase of the oscillation was reversed by artificial hyperpolarization of the membrane past the reversal potential for fast inhibitory postsynaptic potentials (IPSPs). Thus this oscillation was attributed to the action of rhythmic IPSPs activated only during the depolarizing episodes. During the depolarizing episodes, the input resistance of the neurons was decreased and the level of synaptic noise was increased, suggesting that these are periods of increased synaptic activity. 5. Stimulation of CST cells via their axon collaterals in the contralateral neostriatum or cortex produced excitatory synaptic responses in both CST and PT cells, followed by fast inhibitory synaptic potentials. These were followed by a period of prolonged hyperpolarization and a subsequent depolarization. The late phases of the response had the same characteristics as the spontaneous periods of hyperpolarization and depolarization. This pattern of activity in corticostriatal cells is as expected on the basis of responses of neostriatal cells to similar stimulation and is sufficient to account for the pattern seen in the neostriatum. Similar responses were seen on stimulation of the ventrolateral nucleus of the thalamus. 6. The coordinated late polarized and depolarized responses seen in corticostriatal neurons after thalamic or contralateral striatal stimulation generate the coherent discharge of large numbers of corticostriatal neurons required to account for the responses of neostriatal spiny neurons. The spontaneous depolarizations and firing in corticostriatal neurons, if it is similarly correlated, could produce the episodes of converging synaptic excitation previously proposed to account for the firing patterns of neostriatal cells.