Differential morphology of pyramidal tract‐type and intratelencephalically projecting‐type corticostriatal neurons and their intrastriatal terminals in rats

Abstract

Two types of corticostriatal projection neurons have been identified: 1) one whose intrastriatal arborization arises as a collateral of a projection to the ipsilateral brainstem via the pyramidal tract (PT-type); and 2) one that projects intratelencephalically to the cortex and striatum, in many cases bilaterally, but not extratelencephalically (IT-type). To assess possible functional differences between these two neuron types, we characterized their laminar location in the cortex, their perikaryal size, and the morphology of their intrastriatal terminals. IT-type neurons were retrogradely labeled by tetramethylrhodamine-dextran amine (RDA)3k injection into the contralateral striatum, whereas their intrastriatal terminals were labeled anterogradely by biotinylated dextran amine (BDA)10k injection into the contralateral motor or primary somatosensory cortex. To label PT-type neurons and their ipsilateral intrastriatal terminals retrogradely, BDA3k was injected into the pontine pyramidal tract. We found that IT-type neuronal perikarya are medium-sized (12-13 microm) and located in layer III and upper layer V, whereas PT-type perikarya are larger (18-19 microm) and most commonly located in lower layer V. At the electron microscopic level, the intrastriatal terminals of both corticostriatal neuron types made asymmetric synaptic contact with spine heads and less frequently with dendrites. IT-type axospinous terminals were characteristically small (0.4-0.5 microm) and regular in shape, whereas PT-type terminals were typically large (0.8-0.9 microm) and often irregular in shape. Perforated postsynaptic densities were common for PT-type terminals, but not IT-type. The clear differences between these two corticostriatal neuron types in perikaryal size and laminar location in the cortex, and in the size and shape of their intrastriatal terminals, suggest that they may differ in the nature of their influence on the striatum.

Recurrent Connection Patterns of Corticostriatal Pyramidal Cells in Frontal Cortex

“…Direct pathway cells are considered to promote desired movements, and GPe-exclusive cells are considered to inhibit unwanted movement (Albin et al, 1989;DeLong, 1990;Lei et al, 2004). Recently, it has been revealed that two types of corticostriatal cells differentially innervate one of the above two striatal output cells (Reiner et al, 2003;Lei et al, 2004). In light of these data, it is likely that CPn cells preferentially innervate GPe-exclusive cells while CCS cells innervate direct pathway cells.…”

Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats

“…This input primarily ends as terminals that make asymmetric synaptic contact with dendritic spines of striatal projection neurons, which make up ϳ95% of striatal neurons (Albin et al, 1989;Reiner and Anderson, 1990;Gerfen, 1992). In each cortical region, two types of corticostriatal neuron can be distinguished (Wilson, 1987;Cowan and Wilson, 1994;Wright et al, 1999Wright et al, , 2001Reiner et al, 2003). One type, which we refer to as the pyramidal tract (PT)-type, possesses 15-20 m perikarya found primarily in lower layer V, and their striatal projection arises as a collateral of the main axon as it traverses striatum in its course to the ipsilateral pyramidal tract (Wilson, 1987;Cowan and Wilson, 1994;Levesque et al, 1996a,b;Levesque and Parent, 1998;Reiner et al, 2003).…”

“…In each cortical region, two types of corticostriatal neuron can be distinguished (Wilson, 1987;Cowan and Wilson, 1994;Wright et al, 1999Wright et al, , 2001Reiner et al, 2003). One type, which we refer to as the pyramidal tract (PT)-type, possesses 15-20 m perikarya found primarily in lower layer V, and their striatal projection arises as a collateral of the main axon as it traverses striatum in its course to the ipsilateral pyramidal tract (Wilson, 1987;Cowan and Wilson, 1994;Levesque et al, 1996a,b;Levesque and Parent, 1998;Reiner et al, 2003). The second type projects to basal ganglia and cortex but not outside telencephalon.…”

“…The second type projects to basal ganglia and cortex but not outside telencephalon. These neurons, which we refer to as the intratelencephalically projecting (IT)-type, possess 12-15 m perikarya found mainly in layer III and upper layer V (Landry et al, 1984;Wilson, 1987;Cowan and Wilson, 1994;Levesque et al, 1996a,b;Levesque and Parent, 1998;Wright et al, 1999Wright et al, , 2001Reiner et al, 2003).…”

“…IT-type neurons project to ipsilateral striatum, as well as contralateral in many cases, and have a uniform intrastriatal arborization with sparse en passant terminals over a 1.5 mm expanse (Wilson, 1987;Cowan and Wilson, 1994;Wright et al, 1999Wright et al, , 2001. Previously (Reiner et al, 2003), we noted that axospinous PT-type terminals in rat striatum are typically large (0.82 m in mean diameter) and irregular in shape, whereas axospinous IT-type terminals are characteristically small (average diameter of 0.41 m) and regular in shape (round or oval). Wright et al (1999Wright et al ( , 2001) reported similar findings.…”