Novel and Distinct Operational Principles of Intralaminar Thalamic Neurons and Their Striatal Projections

Abstract

Neurons of the intralaminar thalamus, including central lateral (CL) and parafascicular (Pf) nuclei, innervate the cortex and striatum and are important for cognitive, sensory, and motor processes. We tested the hypothesis that CL and Pf neurons provide functionally distinct inputs to the striatum. We performed recordings of single CL and Pf neurons in anesthetized rats and, after juxtacellularly labeling the neurons, their somatodendritic features and synaptic connections were characterized.All CL neurons (n ϭ 31) discharged classic low-threshold Ca 2ϩ spike bursts during cortical slow-wave activity in vivo. In contrast, Pf neurons (n ϭ 52) rarely fired such bursts, but instead discharged groups of spikes at relatively low frequencies. The activity of CL and Pf neurons was often temporally coupled to cortical slow oscillations. Identified CL neurons possessed archetypal "bushy" dendrites and preferentially established synapses with dendritic spines (91% of synapses) of striatal projection neurons. Pf neurons possessed "reticular-like" dendrites, and, on average, preferentially established synapses with dendritic shafts (63%) in striatum, although connectivity was markedly heterogeneous across neurons. Two of the six Pf neurons studied exclusively targeted dendritic shafts, whereas another neuron almost exclusively (97%) targeted spines. The remaining three neurons preferentially targeted dendritic shafts (53-70%).Thus, the fundamental properties of CL and Pf neurons differ (the latter do not express the typical operational principles of thalamic relay neurons), and they provide different temporally patterned inputs to distinct striatal targets. This mechanistic diversity likely underpins the transmission of specific and discrete information from intralaminar thalamic nuclei to striatal and cortical targets.

A Dopaminergic Axon Lattice in the Striatum and Its Relationship with Cortical and Thalamic Terminals

“…Furthermore, long and short term plasticity of thalamostriatal synapses (Smeal et al, 2007;Ding et al, 2008;Raju et al, 2008), like that of the corticostriatal synapses, is likely, at least in part, to be dependent on released dopamine. These findings, together with those of previous studies (Dubé et al, 1988;Xu et al, 1991;Lapper and Bolam, 1992;Lacey et al, 2005Lacey et al, , 2007McHaffie et al, 2005;Raju et al, 2006), suggest that the thalamostriatal projections exhibit a rich and diverse complexity of function on a par with that of the corticostriatal projections.…”

Cortical and Thalamic Innervation of Direct and Indirect Pathway Medium-Sized Spiny Neurons in Mouse Striatum

“…With sufficient convergent excitatory input and appropriate modulatory influence of released dopamine, the selected population of MSNs, which likely constitute both direct and indirect pathway neurons, will fire action potentials, and it is this that underlies basal gangliaassociated behavior. Our findings, together with those of others, suggest that, although the thalamostriatal pathway carries different functional information from that of the corticostriatal pathway and encodes it in an heterogeneous manner (Lacey et al, 2007) that is distinct from the cortex in terms of receptor profiles, release probability, and short-term plasticity (Ding et al, 2008;Smeal et al, 2008), it is likely to be equally involved in the selection of individual or populations of MSNs of both the direct and indirect pathways.…”

“…Of course, a notable exception is the thalamostriatal pathway originating in the parafascicular nucleus, which principally innervates dendritic shafts (Raju et al, 2006;Lacey et al, 2007). The spatial relationship between thalamostriatal synapses and dopaminergic synapses is similar to the relationship between corticostriatal and dopaminergic synapses; thus, both are in a position to be modulated by released dopamine to a similar degree (Moss and Bolam, 2008).…”

“…Any specific differences between corticostriatal and thalamostriatal projections are likely to be underscored by the particular neurons within different functional regions of the cortex or subnuclei thalamus that give rise to the projections. The thalamostriatal projection, in particular, is highly heterogeneous with respect to the somatodendritic morphology of the projecting neurons, their electrophysiological activity, synaptic targets, and patterns of innervation of the matrix and patch/striosomes (Herkenham and Pert, 1981;Deschênes et al, 1996;Smith et al, 2004;Raju et al, 2006;Lacey et al, 2007).…”

An Essential Role for Frizzled5 in Neuronal Survival in the Parafascicular Nucleus of the Thalamus

“…The PFN and the adjacent centromedian nucleus provide major noncortical glutamatergic input to the striatum (Royce and Mourey, 1985;Sadikot et al, 1992a,b;Deschenes et al, 1996;Matsumoto et al, 2001;Yasukawa et al, 2004;Lacey et al, 2007;Smeal et al, 2007). The PFN also projects to the motor and anterior cingulate cortices (Vercelli et al, 2003;Parent and Parent, 2005).…”