Differential processing of thalamic information via distinct striatal interneuron circuits

Abstract

Recent discoveries of striatal GABAergic interneurons require a new conceptualization of the organization of intrastriatal circuitry and their cortical and thalamic inputs. We investigated thalamic inputs to the two populations of striatal neuropeptide Y (NPY) interneurons, plateau low threshold spike (PLTS) and NPY-neurogliaform (NGF) cells. Optogenetic activation of parafascicular inputs evokes suprathreshold monosynaptic glutamatergic excitation in NGF interneurons and a disynaptic, nicotinic excitation through cholinergic interneurons. In contrast, the predominant response of PLTS interneurons is a disynaptic inhibition dependent on thalamic activation of striatal tyrosine hydroxylase interneurons (THINs). In contrast, THINs do not innervate NGF or fast spiking interneurons, showing significant specificity in THINs outputs. Chemospecific ablation of THINs impairs prepulse inhibition of the acoustic startle response suggesting an important behavioural role of this disynaptic pathway. Our findings demonstrate that the impact of the parafascicular nucleus on striatal activity and some related behaviour critically depend on synaptic interactions within interneuronal circuits.

Excitatory extrinsic afferents to striatal interneurons and interactions with striatal microcircuitry

“…Furthermore, thalamostriatal synapses exhibit more prominent AMPA receptor‐mediated currents than corticostriatal synapses (Sciamanna et al ., ). We and others have also shown that optogenetic stimulation of terminals from the PfN as well as from cortex was able to induce action potential firing of FSI in mouse striatal slices (Arias‐Garcia et al ., ; Assous et al ., ).…”

“…Those results, using different manipulations of the PfN, implicate different excitatory and inhibitory components of the CIN response to PfN activation which likely explain the discrepancies. Together with recent data showing that different populations of GABAergic interneurons innervate CINs (English et al ., ) as well as receive monosynaptic inputs from PfN (Assous et al ., ), it seems clear that intrastriatal circuitry plays an critical role in the response of CIN to extrinsic glutamatergic inputs.…”

“…THINs receive monosynaptic glutamatergic cortical inputs and respond to cortical electrical stimulation with EPSPs that elicit spiking (Ibanez‐Sandoval et al ., ). In a recent study, we also investigated the thalamic input from the PfN to THINs (Assous et al ., and unpublished data). We found that optogenetic stimulation of the PfN evoked large excitatory responses in all THINs which almost always gave rise to an action potential.…”

“…Stimulation of thalamus and cortex can produce monosynaptic excitatory responses in the same CIN (Wilson et al ., ; Doig et al ., ). However, both anatomical and physiological studies have shown that the innervation from the thalamus and especially the intralaminar thalamic nuclei is stronger than the relatively weaker cortical innervation of CINs (Meredith & Wouterlood, ; Lapper & Bolam, ; Ding et al ., ; Doig et al ., ; Assous et al ., ). Electrical stimulation of the parafascicular nucleus modulates acetylcholine release in vivo measured by in vivo microdialysis (Consolo et al ., ; Zackheim & Abercrombie, ; Nanda et al ., ).…”

Integrated anatomical and physiological mapping of striatal afferent projections

“…K). These results are consistent with recent studies of the excitatory‐inhibitory control of LTSI activity by PFas projections (Assous et al ., ), but conflict with other anatomical and optogenetic data (Kachidian et al ., ; Ellender et al ., ). The mechanistic basis of these anatomical–physiological discrepancies is currently unclear but could relate to the presence of silent synapses or a sparse distribution of connectivity due to lower density of striatal‐projecting PFas axons or target specificity within patch‐matrix compartments (Herkenham & Pert, ; Deschenes et al ., ).…”