Neural mechanisms for filtering self-generated sensory signals in cerebellum-like circuits

Requarth, Tim; Sawtell, Nathaniel B.

doi:10.1016/j.conb.2011.05.031

Cited by 75 publications

(63 citation statements)

References 42 publications

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“…Recent work in a cerebellum-like structure in the electric fish suggest that diverse intrinsic properties of local circuit neurons may function to expand the repertoire of granule cell responses to stereotyped inputs (Requarth and Sawtell 2011). The resulting large population of granule cell responses enables that brain region to efficiently generate "negative images" of sensory input which could be subtracted at the next cell layer, yielding derivative-like neural signals that emphasize the unexpected components of the sensory response.…”

Section: Functional Significance Of Golgi Cells In the Olfactory Bulbmentioning

confidence: 99%

Voltage-dependent intrinsic bursting in olfactory bulb Golgi cells

2013

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In the mammalian olfactory bulb (OB), local synaptic circuits modulate the evolving pattern of activity in mitral and tufted cells following olfactory sensory stimulation. GABAergic granule cells, the most numerous interneuron subtype in this brain region, have been extensively studied. However, classic studies using Golgi staining methods identified many other, nongranule cell types in the OB whose function remains mysterious. Within just the granule cell layer (GCL), Ramón y Cajal described multiple morphologically distinct subtypes of nongranule interneurons including large spiny Blanes cells which exhibit intrinsic persistent activity. Here, we define the intrinsic electrophysiology of a different nongranule interneuronal cell type in the GCL described by Ramón y Cajal, sparsely spiny Golgi cells in the rat OB. Golgi cells exhibit two distinct firing modes depending on the membrane potential: tonic firing and bursting. Golgi cells also generate rebound bursts following the offset of hyperpolarizing steps. We find that both low-threshold burst responses to depolarizing inputs and rebound bursts are blocked by nickel, an antagonist of T-type voltage-gated Ca2+ current. The state-dependent firing behavior we report in OB Golgi cells suggests that the function of these interneurons may dynamically shift from providing rhythmic potent inhibition of postsynaptic target neurons at sniffing frequencies to tonic, subtractive inhibition based on centrifugal modulatory input.

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Section: Functional Significance Of Golgi Cells In the Olfactory Bulbmentioning

confidence: 99%

Voltage-dependent intrinsic bursting in olfactory bulb Golgi cells

2013

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“…Research on the sensory processing of electric signals quickly gained traction and expanded rapidly with momentum that continues today (e.g. Chacron et al, 2011;Pereira and Caputi, 2010;Requarth and Sawtell, 2011). Similarly, steady and growing progress is evident in the extensive work on central mechanisms controlling EOD rate, especially in the contexts of social communication (reviewed by Lorenzo et al, 2006;Scheffel and Kramer, 2006).…”

Section: Introductionmentioning

confidence: 99%

Electrocyte physiology: 50 years later

Markham

2013

Journal of Experimental Biology

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SummaryWeakly electric gymnotiform and mormyrid fish generate and detect weak electric fields to image their worlds and communicate. These multi-purpose electric signals are generated by electrocytes, the specialized electric organ (EO) cells that produce the electric organ discharge (EOD). Just over 50years ago the first experimental analyses of electrocyte physiology demonstrated that the EOD is produced and shaped by the timing and waveform of electrocyte action potentials (APs). Electrocytes of some species generate a single AP from a distinct region of excitable membrane, and this AP waveform determines EOD waveform. In other species, electrocytes possess two independent regions of excitable membrane that generate asynchronous APs with different waveforms, thereby increasing EOD complexity. Signal complexity is further enhanced in some gymnotiforms by the spatio-temporal activation of distinct EO regions with different electrocyte properties. For many mormyrids, additional EOD waveform components are produced by APs that propagate along stalks that connect postsynaptic regions to the main body of the electrocyte. I review here the history of research on electrocyte physiology in weakly electric fish, as well as recent discoveries of key phenomena not anticipated during early work in this field. Recent areas of investigation include the regulation of electrocyte activity by steroid and peptide hormones, the molecular evolution of electrocyte ion channels, and the evolutionary selection of ion channels expressed in excitable cells. These emerging research areas have generated renewed interest in electrocyte function and clear future directions for research addressing a broad range of new and important questions.

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“…Although again not necessarily mutually exclusive, some of these speculations assert that the cerebellum as a whole implements a form of "internal model" representation for ideal movements (Lisberger 2009), while others suggest that the molecular layer represents a form of adaptive filter, relating sensory input to motor output (Dean et al 2010b;Requarth and Sawtell 2011).…”

Section: Motor Control As the Computational Context For Cerebellar Thmentioning

confidence: 99%

“…Regardless of whether models or theories assume the molecular layer implements a timing (Carrillo et al 2008;D'Angelo and De Zeeuw 2009;Dean and Porrill 2008;Dean et al 2010b;Heck et al 2007;Ioffe et al 2007;Jacobson et al 2008;Kawato and Gomi 1992;Kitazawa and Wolpert 2005;Ohyama et al 2003;Yamazaki and Tanaka 2009), or learning function (Apps and Garwicz 2005;Bell et al 2008;D'Angelo and De Zeeuw 2009;Dean et al 2010b;Empson and Knopfel 2010;Ito 2006;Kitazawa and Wolpert 2005;Lisberger 2009;Molinari et al 2007;Ohyama et al 2010;Shadmehr and Krakauer 2008) or some combination of the two, or implements an adaptive filter (Dean et al 2010b;Requarth and Sawtell 2011) or an inverse kinematic model (Lisberger 2009), or some combination of the two, all existing algorithmic speculations regarding molecular layer circuitry make one overarching assumption: that parallel fiber input directly drives Purkinje cell output. While it seems reasonable to assume that an excitatory input as massive as that of the parallel fibers would directly drive somatic spiking, the experimental fact is that there is little experimental evidence that they do (Bell and Grimm 1969;Bower and Woolston 1983;Brown and Ariel 2009;Chu et al 2011a, b;Cohen and Yarom 1998;De Jaeger and Proteau 2003;de Solages et al 2008;Dizon and Khodakhah 2011;Eccles et al 1972b;Heck et al 2007;…”

Section: What Do Parallel Fibers Do To Purkinje Cells?mentioning

confidence: 99%

Computational Structure of the Cerebellar Molecular Layer

Bower¹

2013

Handbook of the Cerebellum and Cerebellar Disorders

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Theories regarding the computational structure of the cerebellar molecular layer have been more strongly influenced by biological data than is the case for many and perhaps even most other vertebrate brain regions. Yet, or perhaps for this reason, the computational significance of this circuitry remains a very active subject of discussion and debate, with even basic assumptions regarding the physiological organization of this circuit now being questioned. Specifically, while most current models of molecular layer circuitry assume that parallel fiber excitatory synaptic input directly drives Purkinje cells to fire, there is growing experimental evidence that this might not be the case. Recent model-based efforts to better understand the functional role of the parallel fiber system suggest that molecular layer inhibition may play a larger and more complex physiological role than previously realized. In turn, this reanalysis of the role of inhibition in cerebellar cortical circuitry suggests that the cerebellar molecular layer may implement a sensory-related contextual algorithm, rather than either a timing or associative learning function previously assumed to provide the basis for a cerebellar involvement in motor coordination.

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Neural mechanisms for filtering self-generated sensory signals in cerebellum-like circuits

Cited by 75 publications

References 42 publications

Voltage-dependent intrinsic bursting in olfactory bulb Golgi cells

Voltage-dependent intrinsic bursting in olfactory bulb Golgi cells

Electrocyte physiology: 50 years later

Computational Structure of the Cerebellar Molecular Layer

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