Concurrent Thalamostriatal and Corticostriatal Spike-Timing-Dependent Plasticity and Heterosynaptic Interactions Shape Striatal Plasticity Map

Abstract

The striatum integrates inputs from the cortex and thalamus, which display concomitant or sequential activity. The striatum assists in forming memory, with acquisition of the behavioral repertoire being associated with corticostriatal (CS) plasticity. The literature has mainly focused on that CS plasticity, and little remains known about thalamostriatal (TS) plasticity rules or CS and TS plasticity interactions. We undertook here the study of these plasticity rules. We found bidirectional Hebbian and anti-Hebbian spike-timing-dependent plasticity (STDP) at the thalamic and cortical inputs, respectively, which were driving concurrent changes at the striatal synapses. Moreover, TS- and CS-STDP induced heterosynaptic plasticity. We developed a calcium-based mathematical model of the coupled TS and CS plasticity, and simulations predict complex changes in the CS and TS plasticity maps depending on the precise cortex–thalamus–striatum engram. These predictions were experimentally validated using triplet-based STDP stimulations, which revealed the significant remodeling of the CS-STDP map upon TS activity, which is notably the induction of the LTD areas in the CS-STDP for specific timing regimes. TS-STDP exerts a greater influence on CS plasticity than CS-STDP on TS plasticity. These findings highlight the major impact of precise timing in cortical and thalamic activity for the memory engram of striatal synapses.

Heterosynaptic Plasticity and the Experience-Dependent Refinement of Developing Neuronal Circuits

“…However, it is distinct from homeostatic plasticity as the depression arises through LTP induction rather than a change in postsynaptic firing rate, occurs specifically for the unstimulated pathway, and occurs rapidly on a similar timescale with homosynaptic potentiation. Compensatory heterosynaptic plasticity occurring alongside homosynaptic plasticity has since been observed between inputs synapsing onto the same neuron (Royer and Paré, 2003 ; Bian et al, 2015 ; Oh et al, 2015 ; Jungenitz et al, 2018 ; Field et al, 2020 ; Mendes et al, 2020 ; Tong et al, 2021 ), and can also occur following homosynaptic LTD with compensatory heterosynaptic potentiation (H-LTP; Royer and Paré, 2003 ; Field et al, 2020 ). The change in the weight of inactive synapses does not always occur in the opposite direction of homosynaptic change, but can instead be dependent on the initial synaptic weight of the inactive synapse, with strong inactive inputs depressed and weak inactive synapses potentiated or left unchanged (Letellier et al, 2016 ; Bannon et al, 2017 ; Chistiakova et al, 2019 ; Field et al, 2020 ).…”

“…While this review has focused on the development of V1 and ODP in particular, it is equally important to examine the role of heterosynaptic plasticity in the development of other brain regions (Royer and Paré, 2003 ; Chu et al, 2015 ; Field et al, 2020 ; Mendes et al, 2020 ). While many functions of heterosynaptic plasticity in development are likely to be generalizable; from previous studies we expect plasticity rules to vary between different neuron types, brain regions, and developmental stages.…”

“…In V1, heterosynaptic plasticity of non-stimulated inputs on fast-spiking interneurons functions to renormalize net input while in non-fast spiking interneurons heterosynaptic change is instead biased towards overall potentiation (Chistiakova et al, 2019 ). In the striatum, heterosynaptic plasticity rules differ between dopamine receptor 2 expressing and non-expressing medium spiny neurons (Mendes et al, 2020 ). In CA1, the spread of heterosynaptic plasticity through Ca 2+ induced Ca 2+ release declines over development (Lee et al, 2016 ), and in adult-born dentate granule cells, homosynaptic plasticity appears approximately 7 days prior to heterosynaptic plasticity and does not fully develop until much later (Jungenitz et al, 2018 ).…”

Brain is modulated by neuronal plasticity during postnatal development

“…Similar spike-timing-dependent plasticity (STDP) is a biological process that modulates the neural synaptic strength in the brain. This can lead to bidirectional corticostriatal (CS) and thalamostriatal (TS) STDP as anti-Hebbian CS-STDP and Hebbian TS-STDP [29] in physiological conditions without blocking the GABAergic transmission in the dorsolateral striatum [30][31][32][33].…”

What Is the Role of Thalamostriatal Circuits in Learning Vocal Sequences?

“…Aside from signaling through ChIs, thalamostriatal circuits also provide abundant direct inputs onto MSNs (Figure 1D; Lacey et al, 2007;Smith et al, 2009;Guo et al, 2015). Thus, thalamostriatal activity might have a significant direct influence on spike-timingdependent plasticity (STDP) at corticostriatal synapses (Mendes et al, 2020). In addition, the distribution of cell types in Area X receiving direct input from DLM and/or DTZ remains FIGURE 3 | Hypothetical scenarios for learning syllable transitions.…”