Connectivity and Convergence of Single Corticostriatal Axons

Abstract

The distribution of synapses formed by corticostriatal neurons was measured to determine the average connectivity and degree of convergence of these neurons and to search for spatial inhomogeneities. Two kinds of axonal fields, focal and extended, and two striatal tissue compartments, the patch (striosome) and matrix, were analyzed separately. Electron microscopic examination revealed that both kinds of corticostriatal axons made synapses at varicosities that could be identified in the light microscope, and each varicosity made a single synapse. Thus, the distribution of varicosities was a good estimate of the spatial distribution of synapses. The distance between axonal varicosities was measured to determine the density of synaptic connections formed by one axon within the volume occupied by a striatal neuron. Intersynaptic distances were distributed exponentially, except that synapses were rarely located Ͻ4 m apart. The mean distance between synapses was ϳ10 m, so axons made a maximum of 40 synapses within the dendritic volume of a spiny neuron. There are ϳ2840 spiny neurons located within the volume of the dendrites of one spiny cell (Oorschot, 1996), so each axon must contact Յ1.4% of all cells in its axonal arborization. Within the same volume there are ϳ30.5 million asymmetric synapses (Ingham et al., 1996), approximately half of which are cortical in origin. Thus, ϳ380,000 cortical axons innervate the volume of the dendritic tree of one spiny cell. Striatal neurons with totally overlapping dendritic volumes have few presynaptic cortical axons in common, and cortical cells with overlapping axons have few striatal target neurons in common. These results explain the absence of redundancy in the responses of neurons located near each other in the striatum.Key words: cerebral cortex; neostriatum; synapse; axonal arborization; neuronal connectivity; convergence; divergence Since the pioneering work of Webster (1961), cortical afferents to the neostriatum have been known to maintain an orderly spatial map of the cortex within the three dimensional structure of the neostriatum. Although early studies of the nature of the corticostriatal projection suggested that it was a continuous one in which near neighbors in the cortex are connected to near neighbors in the neostriatum (Kemp and Powell, 1970), more recent findings have shown it to be essentially discontinuous (Selemon and Goldman-Rakic, 1985;Malach and Graybiel, 1986). The discontinuities are most clearly shown in axonal tracing studies from physiologically characterized cortical regions performed by Graybiel (1991, 1993a) and Parthasarathy et al. (1992). These experiments show that individual locations in the cortex give rise to multiple separate foci of innervation in the neostriatum and that axons from f unctionally related cortical regions (e.g., the finger area of primary motor and somatosensory cortex) share common focal innervation zones. Subsequent studies of the arborization patterns of single corticostriatal cells have shown that many of these mak...

Dopaminergic Modulation of Axon Collaterals Interconnecting Spiny Neurons of the Rat Striatum

“…Therefore, an average of five boutons per connection is a reasonable number (quantum, 10 -20 pA, depending on intracellular Cs ϩ ). Similar stimulation parameters yielded an average IPSC of 93 pA (20 -500 pA) for intrastriatal inhibition, suggesting that axon collateral inhibition is quantitatively less than interneuron inhibition; however, a spiny neuron receives ϳ10,000 asymmetrical (Kincaid et al, 1998) and ϳ2500 symmetrical synapses (Ingham et al, 1998). Symmetrical synapses can be dopaminergic, cholinergic, or GABAergic, with dopaminergic being ϳ13% (Roberts et al, 2002).…”

“…How many come from axon collaterals? There are ϳ2840 striatal neurons inside the volume of a spiny dendritic tree (Oorschot, 1996;Kincaid et al, 1998). Most spiny neurons have their axon collaterals restricted to this volume (Kawaguchi et al, 1990).…”

Competition between Feedback Loops Underlies Normal and Pathological Dynamics in the Basal Ganglia

“…Recent estimates of connectivity from cortex to striatum and STN indicate that the number of cortical neurons connected to given neurons in these two structures are in the order of K StrCtx ϭ 5000 (Kincaid et al, 1998) and K STNCtx ϭ 100 (Mink, 1996), respectively. The connectivity from the striatum to the GPi, the STN to GPi, and the GPi to the thalamus are less well known.…”

On the Activity of the Corticostriatal Networks during Spike-and-Wave Discharges in a Genetic Model of Absence Epilepsy

“…First, CS neurons provide powerful excitatory synaptic inputs to SONs (Kincaid et al, 1998;Zheng and Wilson, 2002) responsible for the large spontaneous synaptic depolarizations observed in these neurons in vivo (Wilson, 1995;Wilson and Kawaguchi, 1996;Stern et al, 1997;Charpier et al, 1999;Mahon et al, 2001). Second, the strength of association between cortical field potentials and synaptic depolarizations in SONs was dramatically increased during SWDs.…”

“…Synaptic inputs to SONs include glutamatergic excitatory inputs arising from a large number of convergent corticostriatal (CS) neurons (Wilson, 1995;Kincaid et al, 1998;Zheng and Wilson, 2002) and inhibitory connections originating from both collateral interactions between SONs (Czubayko and Plenz, 2002;Tunstall et al, 2002) and GABAergic striatal interneurons (Plenz and Kitai, 1998; Koó s and Tepper, 1999), which also receive powerful excitatory cortical inputs (Kita, 1993;Ramanathan et al, 2002). Given the functional impact of the corticostriatal projections on the excitability of SONs, the cortical paroxysms associated with absence seizures could produce significant changes in the firing pattern of SONs, which could lead to positive or negative modulation of SWDs.…”