Bidirectional Activity-Dependent Plasticity at Corticostriatal Synapses

Abstract

Corticostriatal projections originate from the entire cerebral cortex and provide the major source of glutamatergic inputs to the basal ganglia. Despite the importance of corticostriatal connections in sensorimotor learning and cognitive functions, plasticity forms at these synapses remain strongly debated. Using a corticostriatal slice preserving the connections between the somatosensory cortex and the target striatal cells, we report the induction of both non-Hebbian and Hebbian forms of long-term potentiation (LTP) and long-term depression (LTD) on striatal output neurons (SONs). LTP and LTD can be induced selectively by different stimulation patterns (highfrequency trains vs low-frequency pulses) and were evoked with similar efficiency in non-Hebbian and Hebbian modes. Combination of LTP-LTD and LTD-LTP sequences revealed that bidirectional plasticity occurs at the same SONs and provides efficient homeostatic mechanisms leading to a resetting of corticostriatal synapses avoiding synaptic saturation. The effect of temporal relationship between cortical stimulation and SON activity was assessed using spike-timing-dependent plasticity (STDP) protocols. An LTP was observed when an action potential was triggered in the striatal neuron before the cortical stimulus, and, conversely, an LTD was induced when the striatal neuron discharge was triggered after the cortical stimulation. Such STDP was reversed when compared with those described so far in other mammalian brain structures. This mechanism may be essential for the role of the striatum in learning of motor sequences in which sensory and motor events are associated in a precise time sequence.

Internalized Timing of Isochronous Sounds Is Represented in Neuromagnetic Beta Oscillations

“…This finding is in agreement with the current model of a functional network that modulation of synchrony is a mechanism of dynamic network reconfiguration (Womelsdorf et al, 2007). Mechanisms underlying the beta dynamics could be a frequency transition of oscillatory circuits through synaptic coupling alterations (Kopell et al, 2000;Jensen et al, 2005), changes in nonsynaptic coupling through gap junction conductance in cortical neurons (Roopun et al, 2006), and synaptic plasticity in cortico-striatum connections (Fino et al, 2005). The latter is particularly interesting in that the striato-thalamo-cortical circuit is involved in coincidence detection of oscillatory activities for temporal coding (Matell and Meck, 2004).…”

Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

“…Such rules have first been described in mormyrid electric fish (36) where they explain the formation of negative mirror images (corollary discharges) of reafferent (self-generated) sensory input (2). In mammals, a similar rule has been found to describe synaptic connections from cortex to the basal ganglia (37). Thus, a causal inverse may reside in the efferent synapses of a cortical area upstream of the basal ganglia homolog; or, based on anatomy, a causal inverse could be connected to a dopaminergic ventral tegmental area (38,39), thereby establishing a possible link of our findings with reinforcement learning theories (see below).…”

“…On the other hand, the results of ref. 37 reveal that afferent cortical synapses onto striatal neurons also exhibit plasticity in which postsynaptic before presynaptic firing strengthens the synapse, a rule useful for inverse model learning, according to the theory of refs. 23 and 24.…”

A Ca2+Threshold for Induction of Spike-Timing-Dependent Depression in the Mouse Striatum

“…In the striatum, however, the results obtained to date seem contradictory. Fino et al (2005) reported that spike-timedependent LTD (t-LTD) was induced when presynaptic spikes preceded postsynaptic spikes (pre-post timing), and reversed timing (post-pre timing) produced long-term potentiation (t-LTP). In contrast, Pawlak and Kerr (2008) found that pre-post timing caused t-LTP and reverse timing caused t-LTD. Shen et al (2008) found that pre-post protocols produced t-LTP in dopamine D1 receptorexpressing cells, but under dopamine-depleted conditions, D1 cells showed LTD.…”