S. T. Kitai

Disfacilitation and long-lasting inhibition of neostriatal neurons in the rat

SummaryExcitatory postsynaptic potentials evoked in rat neostriatal spiny projections neurons were followed by a long (100–300 ms) period of membrane hyperpolarization, followed in turn by a late depolarization. Concomitant with these changes in membrane potential were inhibition and subsequent excitation of spontaneous firing and excitatory activity evoked from substantia nigra and cerebral peduncle, but not from cortical stimulating sites. Thalamic-evoked excitatory activity was sometimes sensitive and sometimes insensitive to this inhibition, which has previously been believed to result from intrinsic inhibitory synaptic activity among neostriatal neurons. In intracellular recordings from neostriatal neurons in urethane anesthetized rats this longlasting inhibitory response (1) exhibited alterations with intracellularly applied steady currents comparable to those of the EPSP, (2) failed to respond to intracellular injection of chloride ions, (3) was associated with either a decrease or no detectable change in the input conductance of the neurons, and (4) was abolished after lesions that interrupted polysynaptic pathways to neostriatum through intracortical and intrathalamic synaptic circuits. These findings indicate that the long lasting inhibitory portion of the responses of neostriatal neurons arises from a phasic inhibition of tonically active corticostriatal and thalamostriatal neurons and a concurrent decrease in the excitability of polysynaptic pathways converging on neostriatal neurons.

Neuronal interactions in the substantia nigra pars reticulata through axon collaterals of the projection neurons

SummarySubstantia nigra pars reticulata (SNr) neurons, antidromically activated following stimulation of the dorsal thalamus and/or superior colliculus were intracellularly stained with HRP. Light microscopic analysis revealed that the labeled SNr neurons have axon collaterals arborizing within SNr. Axon collaterals of SNr neurons partially overlapped with the dendritic fields of their parent cells and also extended beyond the parent dendritic fields. The labeled axon terminals did not closely appose the parent cell processes, suggesting that the collaterals most likely terminate on neurons other than the parent cell.Electrical stimulation of either the thalamus or the superior colliculus induced monosynaptic and polysynaptic IPSPs in SNr cells. The polysynaptic IPSPs evoked from thalamic stimulation disappeared following hemitransection of the brain just rostral to the thalamus while the monosynaptic IPSPs remained the same. Since there are no known afferents from either thalamus or superior colliculus to SNr, we consider that these monosynaptic IPSPs are due to activation of the recurrent collaterals of SNr projection cells. The results of this study indicate that projection neurons of SNr also have an inhibitory role within the SNr.

Origins of postsynaptic potentials evoked in identified rat neostriatal neurons by stimulation in substantia nigra.

SummaryResponses of striatal neurons to stimulation in substantia nigra were recorded intracellularly in intact rats and after acute or chronic unilateral lesions of cerebral cortex or after combined cortical lesions and unilateral thalamic transections. Spiny striatal efferent neurons were identified by intracellular injection of horseradish peroxidase. In intact animals substantia nigra stimulation evoked a complex response with both excitatory and inhibitory phases. Acute unilateral decortication abolished the inhibitory phase of the response and reduced the amplitude of the initial EPSP. Thus, part of the excitatory phase and most or all of the inhibitory phase of the response result from polysynaptic routes to striatum involving cerebral cortex. The remaining EPSP observed in acute decorticate animals exhibited two components distinguished on the basis of their time courses. The latter of these was abolished by thalamic transections. The earlier component was shown to be a monosynaptic EPSP evoked by axon collaterals of cortical efferent neurons projecting to brainstem and was not observed in animals subjected to chronic decortication. After removal of all of these non-nigral response components a small long latency EPSP could be evoked by nigral stimulation. This EPSP is probably due to activation of dopaminergic nigro-striatal axons.

Origins of post synaptic potentials evoked in spiny neostriatal projection neurons by thalamic stimulation in the rat

SummaryStimulation of thalamic intralaminar nuclei or structures along the intrathalamic trajectory of thalamostriatal axons evoked complex EPSPs and subsequent hyperpolarizations in rat neostriatal spiny neurons identified by intracellular injection of horseradish peroxidase and/or antidromic activation from substantia nigra. In intact urethane-anesthetized rats, the initial EPSP portion of the response consisted of several components and lasted up to 75 ms. Short (1–10 ms) latency components exhibiting latency variations suggestive of a polysynaptic origin were often observed, and sometimes were the earliest components of the response. However, individual components of the excitatory response could not be clearly distinguished in most neurons and the earliest excitatory component usually appeared to be monosynaptic.After large acute aspiration lesions of ipsilateral cerebral cortex, the early polysynaptic EPSP components of thalamic-evoked EPSPs were absent or greatly attenuated. This suggested that most or all of the short latency polysynaptic EPSP components arose via a thalamo-cortico-striatal route. A short latency (1.6–4.0 ms) monosynaptic EPSP and a second excitatory component with a longer and more variable latency (8–28 ms) remained intact after acute decortication. These were not dependent upon intact corticothalamic or corticostriatal axons, since they were both still present in experiments performed as long as 4 days following ipsilateral hemidecortication. The longer latency excitatory response was shown to be polysynaptic by its latency variation with changes in stimulus intensity and frequency. This component of the response was abolished after acute thalamic hemitransections separating thalamostriatal neurons from their axons. In these experiments, stimulation of thalamostriatal axons rostral to the transection continued to evoke monosynaptic EPSPs in neostriatal spiny neurons. These EPSPs ranged from 1.8 to 3.0 ms in latency, had peak amplitudes up to 11 mV and were 20–37 ms in duration.