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

1. Spontaneous fluctuations of membrane potential, patterns of spontan eous firing, dendritic branching patterns, and intracortical and stria tal axonal arborizations were compared for two types of corticostriata l neurons in the medial agranular cortex of urethan-anesthetized rats: 1) pyramidal tract (PT) cells identified by antidromic activation fro m the medullary pyramid and 2) crossed corticostriatal (CST) neurons i dentified by antidromic activation from the contralateral neostriatum. The ipsilateral corticostriatal projections of intracellularly staine d PT neurons as well as contralateral corticostriatal neurons were con firmed after labeling by intracellular injection of biocytin. 2. All w ell-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 ar borization 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 intrastria tal axonal arborization. Both subclasses of PT neurons had anatomic an d physiological properties associated with slow PT cells in cats and m onkeys and conduction velocities <10 m/s. All of the PT cells but one were regular spiking cells. The exceptional cell fired intrinsic burst s. 3. Intracellularly stained CST neurons were located in the superfic ial half of layer V and the deep part of layer III. Their layer I apic al dendrites were few and sparsely branched. Their axons gave rise to an extensive arbor of local axon collaterals that distributed in the r egion of the parent neuron, frequently extending throughout the more s uperficial layers, including layer I. Axon collaterals were also trace d to the corpus callosum, as expected from their contralateral project ions, and they contributed axon collaterals to the ipsilateral neostri atum. In the neostriatum, these axons formed extended arborizations sp arsely occupying a large volume of striatal tissue. All CST neurons we re 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 w as relatively constant in each state, and transitions between the depo larized and hyperpolarized states were sometimes periodic with a frequ ency 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 a nd triggered action potentials that locked to the depolarizing peaks o f this rhythm. The phase of the oscillation was reversed by artificial hyperpolarization of the membrane past the reversal potential for fas t inhibitory postsynaptic potentials (IPSPs). Thus this oscillation wa s attributed to the action of rhythmic IPSPs activated only during the depolarizing episodes. During the depolarizing episodes, the input re sistance 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 t he contralateral neostriatum or cortex produced excitatory synaptic re sponses in both CST and PT cells, followed by fast inhibitory synaptic potentials. These were followed by a period of prolonged hyperpolariz ation and a subsequent depolarization. The late phases of the response had the same characteristics as the spontaneous periods of hyperpolar ization and depolarization. This pattern of activity in corticostriata l cells is as expected on the basis of responses of neostriatal cells to similar stimulation and is sufficient to account for the pattern se en in the neostriatum. Similar responses were seen on stimulation of t he ventrolateral nucleus of the thalamus. 6. The coordinated late pola rized and depolarized responses seen in corticostriatal neurons after thalamic or contralateral striatal stimulation generate the coherent d ischarge of large numbers of corticostriatal neurons required to accou nt for the responses of neostriatal spiny neurons. The spontaneous dep olarizations and firing in corticostriatal neurons, if it is similarly correlated, could produce the episodes of converging synaptic excitat ion previously proposed to account for the firing patterns of neostria tal cells.