Evolutionarily conserved differences in pallial and thalamic short-term synaptic plasticity in striatum

Authors


S. Grillner: Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden. Email: sten.grillner@ki.se

Key points

  • Recent studies have shown that the striatum and the basal ganglia are to a remarkable degree conserved throughout the vertebrate phylum.

  • As the basic organization of the neural machinery for action selection is present in the lamprey, it is essential to understand how the striatum is activated.

  • In this study we characterize the pharmacology and synaptic dynamics from the lateral pallium (LPal; cortex) and thalamus (Th), the main excitatory input to the striatum.

  • We show that, as in mammals, the LPal and Th provide glutamatergic excitation to the striatum, but with completely opposite short-term synaptic plasticity due to differences in presynaptic properties.

  • These synaptic differences are also characteristic of the mammalian striatum, suggesting that these are fundamental components of the vertebrate mechanisms for action selection.

Abstract  The striatum of the basal ganglia is conserved throughout the vertebrate phylum. Tracing studies in lamprey have shown that its afferent inputs are organized in a manner similar to that of mammals. The main inputs arise from the thalamus (Th) and lateral pallium (LPal; the homologue of cortex) that represents the two principal excitatory glutamatergic inputs in mammals. The aim here was to characterize the pharmacology and synaptic dynamics of afferent fibres from the LPal and Th onto identified striatal neurons to understand the processing taking place in the lamprey striatum. We used whole-cell current-clamp recordings in acute slices of striatum with preserved fibres from the Th and LPal, as well as tract tracing and immunohistochemistry. We show that the Th and LPal produce monosynaptic excitatory glutamatergic input through NMDA and AMPA receptors. The synaptic input from the LPal displayed short-term facilitation, unlike the Th input that instead displayed strong short-term synaptic depression. There was also an activity-dependent recruitment of intrastriatal oligosynaptic inhibition from both inputs. These results indicate that the two principal inputs undergo different activity-dependent short-term synaptic plasticity in the lamprey striatum. The difference observed between Th and LPal (cortical) input is also observed in mammals, suggesting a conserved trait throughout vertebrate evolution.

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