Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium‐size spiny neurons in the rat neostriatum

Abstract

In order to determine what types of neurons in the striatum receive direct synaptic input from corticostriatal and thalamostriatal fibres and whether these afferents converge on individual striatal neurons, double anterograde labelling of axon terminals was combined with Golgi impregnation at both the light and electron microscopic levels. The area of the central neostriatum that receives input from both the parafascicular nucleus of the thalamus and the somatosensory cortex was identified by retrograde transport of a conjugate of horseradish peroxidase and wheat germ agglutinin (HRP‐WGA). The same region of the neostriatum was studied in rats that had received multiple electrolytic lesions in the somatosensory cortex and also an injection of HRP‐WGA in different parts of the parafascicular nucleus. Sections of this part of the neostriatum were impregnated by the single‐section Golgi procedure after revealing anterogradely transported HRP‐WGA. Twelve Golgi‐impregnated spiny neurons were recovered and examined in the light and electron microscope after gold‐toning. Ten of these neurons were typical very densely spiny medium‐size neurons and they were all found to receive asymmetric synaptic input on dendritic spines from degenerating corticostriatal boutons. However, even though numerous boutons labelled anterogradely by HRP‐WGA from the parafascicular nucleus were found within the dendritic fields of neurons that received cortical input, none of the terminals from the thalamus made synaptic contact with these neurons. Instead, all 96 thalamostriatal boutons studied were found in asymmetric synaptic contact with dendritic shafts of other neurons. Two such neurons that received input from the parafascicular nucleus were Golgi‐impregnated and appeared to be medium‐size spiny neurons, but they had a lower density of spines than the typical very densely spiny neurons. An independent confirmation that the targets of thalamostriatal neurons originating in the parafascicular nucleus are dendritic shafts was provided by studying the boutons labelled following electrolytic lesioning or injection of the lectin Phaseolus vulgaris‐leucoagglutinin (PHA‐L) into this nucleus: these boutons were also found to form asymmetric synaptic contacts with dendritic shafts within the neostriatum. It is concluded that although afferents from the somatosensory cortex and from the parafascicular nucleus converge upon the same part of the neostriatum, they probably do not converge upon the same spiny neurons. The afferents from the neocortex form synapses on the spines of densely spiny medium‐size neurons, whereas terminals originating from neurons in the parafascicular nucleus are in synaptic contact with the dendritic shafts of what appears to be a morphologically distinct type of medium‐size spiny neuron. The integration of the inputs from these two areas probably involves the local axon collaterals of these two types of spiny neuron.