Inhibitory Interactions Between Spiny Projection Neurons in the Rat Striatum

Abstract

The spiny projection neurons are by far the most numerous type of striatal neuron. In addition to being the principal projection neurons of the striatum, the spiny projection neurons also have an extensive network of local axon collaterals by which they make synaptic connections with other striatal projection neurons. However, up to now there has been no direct physiological evidence for functional inhibitory interactions between spiny projection neurons. Here we present new evidence that striatal projection neurons are interconnected by functional inhibitory synapses. To examine the physiological properties of unitary inhibitory postsynaptic potentials (IPSPs), dual intracellular recordings were made from pairs of spiny projection neurons in brain slices of adult rat striatum. Synaptic interactions were found in 9 of 45 pairs of neurons using averages of 200 traces that were triggered by a single presynaptic action potential. In all cases, synaptic interactions were unidirectional, and no bidirectional interactions were detected. Unitary IPSPs evoked by a single presynaptic action potential had a peak amplitude ranging from 157 to 319 microV in different connections (mean: 277 +/- 46 microV, n = 9). The percentage of failures of single action potentials to evoke a unitary IPSP was estimated and ranged from 9 to 63% (mean: 38 +/- 14%, n = 9). Unitary IPSPs were reversibly blocked by bicuculline (n = 4) and had a reversal potential of -62.4 +/- 0.7 mV (n = 5), consistent with GABA-mediated inhibition. The findings of the present study correlate very well with anatomical evidence for local synaptic connectivity between spiny projection neurons and suggest that lateral inhibition plays a significant role in the information processing operations of the striatum.

Increased bradykinesia in Parkinson’s disease with increased movement complexity: elbow flexion–extension movements

“…In addition to the facilitation of desired movements, the model demonstrates that suppression of unwanted movements, as proposed by Mink (1996), may be an important function of the BG. The proposal by Tunstall et al (2002) that lateral inhibition among medium spiny neurons of the striatum serves to focus neural activity to the desired movement is further strengthened by the model. The model also provides support for the functional role of the hyperdirect pathway in the suppression of unwanted movements that could potentially interfere with the planned action, as proposed by Nambu et al (2002).…”

“…Lateral inhibition between modules was implemented at the level of the striatum as there is evidence for inhibitory recurrent connections among striatal projection neurons (Tunstall et al 2002). An additional inhibitory input from the axon collaterals of striatal projection neurons in neighbouring motor modules was included to model this effect, as shown in Fig.…”

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

“…Thus, IPSCs of microvolts or millivolts can be measured when comparing intracellular (Tunstall et al, 2002) with whole-cell (Czubayko and Plenz, 2002) recordings, in both adult and young spiny cells. In voltage-clamp mode, unitary IPSCs range from 20 to 250 pA (Koos et al, 2002); the minimum is in the range of quantal events in other synapses (Hanse and Gustafsson, 2001).…”

“…Inhibition comes from two main sources: interneurons (Kita, 1993;Bennett and Bolam, 1994;Jaeger et al, 1994;Kawaguchi et al, 1995;Koos and Tepper, 1999) and recurrent axon collaterals interconnecting projection neurons (Park et al, 1980;Wilson and Groves, 1980;Somogyi et al, 1981;Bishop et al, 1982;Groves, 1983;Aronin et al, 1986;Bolam and Izzo, 1988;Czubayko and Plenz, 2002;Koos et al, 2002;Tunstall et al, 2002). We asked whether dopamine regulates the strength of synapses between projection neurons.…”

A Critical Interaction between Dopamine D2 Receptors and Endocannabinoids Mediates the Effects of Cocaine on Striatal GABAergic Transmission

“…GABAergic innervation of striatal cells is essentially intrinsic, as recurrent collaterals of projection neurons and GABAergic interneurons virtually represent the totality of their inhibitory inputs (Plenz and Kitai, 1998;Koos and Tepper, 1999;Tunstall et al, 2002). Among the various GABAergic inputs to spiny neurons, those originating from fast-spiking interneurons seem to exert the prominent inhibitory control on the functional activity of these cells (Plenz and Kitai, 1998;Koos and Tepper, 1999).…”