Toward a Neurocentric View of Learning

Titley, Heather K.; Brunel, Nicolas; Hansel, Christian

doi:10.1016/j.neuron.2017.05.021

Cited by 190 publications

(196 citation statements)

References 111 publications

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“…Intrinsic excitability changes may aid in driving memory formation, with synaptic plasticity serving to determine the information content by individual neurons (Titley et al . ). In cerebellar learning, this equates to a scaling of synaptic input weights depending on whether PF synapses contribute to the occurrence of an error.…”

Section: Discussionmentioning

confidence: 97%

“…The details of mismatch at longer intervals could be explained by the involvement of multiple plasticity mechanisms in learning, some of which are triggered at longer time intervals. Indeed, it has been suggested that cerebellar motor learning rests on multiple mechanisms at multiple brain sites (Hansel et al 2001;Freeman & Steinmetz, 2011;Gao et al 2012;Titley et al 2017;Titley et al 2018).…”

Section: Timing Requirements Of Ltd and Learningmentioning

confidence: 99%

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Complex spike clusters and false‐positive rejection in a cerebellar supervised learning rule

Titley

Kislin

Simmons

et al. 2019

The Journal of Physiology

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Key points Spike doublets comprise ∼10% of in vivo complex spike events under spontaneous conditions and ∼20% (up to 50%) under evoked conditions. Under near‐physiological slice conditions, single complex spikes do not induce parallel fibre long‐term depression. Doublet stimulation is required to induce long‐term depression with an optimal parallel‐fibre to first‐complex‐spike timing interval of 150 ms. Abstract The classic example of biological supervised learning occurs at cerebellar parallel fibre (PF) to Purkinje cell synapses, comprising the most abundant synapse in the mammalian brain. Long‐term depression (LTD) at these synapses is driven by climbing fibres (CFs), which fire continuously about once per second and therefore generate potential false‐positive events. We show that pairs of complex spikes are required to induce LTD. In vivo, sensory stimuli evoked complex‐spike doublets with intervals ≤150 ms in up to 50% of events. Using realistic [Ca2+]o and [Mg2+]o concentrations in slices, we determined that complex‐spike doublets delivered 100–150 ms after PF stimulus onset were required to trigger PF‐LTD, which is consistent with the requirements for eyeblink conditioning. Inter‐complex spike intervals of 50–150 ms provided optimal decoding. This stimulus pattern prolonged evoked spine calcium signals and promoted CaMKII activation. Doublet activity may provide a means for CF instructive signals to stand out from background firing.

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Section: Discussionmentioning

confidence: 97%

Section: Timing Requirements Of Ltd and Learningmentioning

confidence: 99%

Complex spike clusters and false‐positive rejection in a cerebellar supervised learning rule

Titley

Kislin

Simmons

et al. 2019

The Journal of Physiology

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“…62,63 ) or on learning-related transcriptional changes other than those mediated by CREB 64,65 (for the potential utility of hypothesized long-term changes in excitability, see ref. 66 ).…”

Section: Discussionmentioning

confidence: 99%

Memory formation depends on both synapse-specific modifications of synaptic strength and cell-specific increases in excitability

et al. 2018

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The modification of synaptic strength produced by long-term potentiation (LTP) is widely thought to underlie memory storage. Indeed, given that hippocampal pyramidal neurons have > 10,000 independently modifiable synapses, the potential for information storage by synaptic modification is enormous. However, recent work suggests that CREB-mediated global changes in neuronal excitability also play a critical role in memory formation. Because these global changes have a modest capacity for information storage compared with that of synaptic plasticity, their importance for memory function has been unclear. Here we review the newly emerging evidence for CREB-dependent control of excitability and discuss two possible mechanisms. First, the CREB-dependent transient change in neuronal excitability performs a memory-allocation function ensuring that memory is stored in ways that facilitate effective linking of events with temporal proximity (hours). Second, these changes may promote cell-assembly formation during the memory-consolidation phase. It has been unclear whether such global excitability changes and local synaptic mechanisms are complementary. Here we argue that the two mechanisms can work together to promote useful memory function.

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“…Healthy and invigorating debates related to the philosophical and the scientific basis of such analyses, with themes ranging from broad discussions on reductionism versus holism (Bennett & Hacker, ; Bickle, ; Jazayeri & Afraz, ; Krakauer, Ghazanfar, Gomez‐Marin, MacIver, & Poeppel, ; Panzeri, Harvey, Piasini, Latham, & Fellin, ) to more focused debates on the specific cellular components that are involved in specific aspects of coding and behavior (Bliss & Collingridge, ; Gallistel, ; Kandel et al, ; Kim & Linden, ; Martin et al, ; Mayford et al, ; Mozzachiodi & Byrne, ; Neves, Cooke, & Bliss, ; Otchy et al, ; Titley, Brunel, & Hansel, ; Zhang & Linden, ), have contributed to our emerging understanding of neural systems and their links to behavior. Several studies have covered the breadth and depth of these debates (Bargmann & Marder, ; Bennett & Hacker, ; Bickle, ; Jazayeri & Afraz, ; Jonas & Kording, ; Kandel et al, ; Katz, ; Kim & Linden, ; Krakauer et al, ; Lazebnik, ; Marder, ; Marder, ; Marder, ; Marder, O'Leary, & Shruti, ; Marder & Thirumalai, ; Mayford et al, ; Panzeri et al, ; Tytell, Holmes, & Cohen, ), and will not be the focus of this review.…”

Section: Degeneracy: Foundations From the Perspective Of An Encodingmentioning

confidence: 99%

“…In other words, the ability to undergo plasticity is an important requirement for it to encode or learn newly available information from the environment. Such plasticity has been shown to be ubiquitous, spanning cellular and network structures across almost all regions, and could be triggered by development (Desai, Cudmore, Nelson, & Turrigiano, ; Desai, Rutherford, & Turrigiano, ; Luo & Flanagan, ; Schreiner & Winer, ; Turrigiano & Nelson, ; White & Fitzpatrick, ), by learning processes (Kandel, ; Kandel et al, ; Kim & Linden, ; Lamprecht & LeDoux, ; Narayanan & Johnston, ; Titley et al, ; Zhang & Linden, ) or by pathological insults (Beck & Yaari, ; Bernard, Shah, & Johnston, ; Brager & Johnston, ; Grant, ; Johnston, Frick, & Poolos, ; Kullmann, ; Lee & Jan, ; Lehmann‐Horn & Jurkat‐Rott, ; Lerche et al, ; Poolos & Johnston, ). A traditional method to study such plasticity mechanisms is to subject neuronal or synaptic structures to specific activity patterns towards understanding the rules for plasticity in specific components.…”

Section: Degeneracy: Foundations From the Perspective Of An Encodingmentioning

confidence: 99%

Degeneracy in hippocampal physiology and plasticity

2019

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Degeneracy, defined as the ability of structurally disparate elements to perform analogous function, has largely been assessed from the perspective of maintaining robustness of physiology or plasticity. How does the framework of degeneracy assimilate into an encoding system where the ability to change is an essential ingredient for storing new incoming information? Could degeneracy maintain the balance between the apparently contradictory goals of the need to change for encoding and the need to resist change towards maintaining homeostasis? In this review, we explore these fundamental questions with the mammalian hippocampus as an example encoding system. We systematically catalog lines of evidence, spanning multiple scales of analysis that point to the expression of degeneracy in hippocampal physiology and plasticity. We assess the potential of degeneracy as a framework to achieve the conjoint goals of encoding and homeostasis without cross‐interferences. We postulate that biological complexity, involving interactions among the numerous parameters spanning different scales of analysis, could establish disparate routes towards accomplishing these conjoint goals. These disparate routes then provide several degrees of freedom to the encoding‐homeostasis system in accomplishing its tasks in an input‐ and state‐dependent manner. Finally, the expression of degeneracy spanning multiple scales offers an ideal reconciliation to several outstanding controversies, through the recognition that the seemingly contradictory disparate observations are merely alternate routes that the system might recruit towards accomplishment of its goals.

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Toward a Neurocentric View of Learning

Cited by 190 publications

References 111 publications

Complex spike clusters and false‐positive rejection in a cerebellar supervised learning rule

Complex spike clusters and false‐positive rejection in a cerebellar supervised learning rule

Memory formation depends on both synapse-specific modifications of synaptic strength and cell-specific increases in excitability

Degeneracy in hippocampal physiology and plasticity

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