Cerebellar Substrates for Error Correction in Motor Conditioning

Gluck, Mark A.; Allen, Merrill J.; Myers, Catherine E.; Thompson, Richard F.

doi:10.1006/nlme.2001.4031

Cited by 43 publications

(34 citation statements)

References 67 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The inhibitory CR is not responsible for the behavioral CR (eye blink) but is responsible for extinction and blocking (error correction) because it depresses activity in the US pathway (climbing fibers) and alters the US information reaching the Purjinke cells and interpositus nucleus, the sites of CS-US convergence (Kim et al, 1998;Gluck et al, 2001;Medina et al, 2002). Likewise, in Pavlovian appetitive preparations, prediction errors (extinction and associative blocking) are associated with alterations in activity of midbrain dopamine neurons so that the omission of an otherwise expected reward suppresses activity of these cells (Schultz and Dickinson, 2000;Waelti et al, 2001;Tobler et al, 2003).…”

Section: Discussionmentioning

confidence: 99%

Opioid Receptors in the Midbrain Periaqueductal Gray Regulate Extinction of Pavlovian Fear Conditioning

McNally¹,

Pigg²,

Weidemann³

2004

J. Neurosci.

105

117

View full text Add to dashboard Cite

Four experiments studied the role of opioid receptors in the midbrain periaqueductal gray matter (PAG), an important structure eliciting conditioned fear responses, in the extinction of Pavlovian fear. Rats received pairings of an auditory conditioned stimulus (CS) with a foot shock unconditioned stimulus (US). The freezing conditioned response (CR) elicited by the CS was then extinguished via nonreinforced presentations of the CS. Microinjection of the opioid receptor antagonist naloxone into the ventrolateral PAG (vlPAG) before nonreinforced CS presentations impaired development of extinction, but such microinjections at the end of extinction did not reinstate an already extinguished freezing CR. This role for opioid receptors in fear extinction was specific to the vlPAG because infusions of naloxone into the dorsal PAG did not impair fear extinction. Finally, the impairment of fear extinction produced by vlPAG infusions of naloxone was dose-dependent. These results show for the first time that the midbrain PAG contributes to fear extinction and specifically identify a role for vlPAG opioid receptors in the acquisition but not the expression of such extinction. Taken together with our previous findings, we suggest that, during fear conditioning, activation of vlPAG opioid receptors contributes to detection of the discrepancy between the actual and expected outcome of the conditioning trial. vlPAG opioid receptors regulate the learning that accrues to the CS and other stimuli present on a trial because they instantiate an associative error correction process influencing US information reaching the site of CS-US convergence in the amygdala. During nonreinforcement, this vlPAG opioid receptor contribution signals extinction.

show abstract

Section: Discussionmentioning

confidence: 99%

Opioid Receptors in the Midbrain Periaqueductal Gray Regulate Extinction of Pavlovian Fear Conditioning

McNally¹,

Pigg²,

Weidemann³

2004

J. Neurosci.

105

117

View full text Add to dashboard Cite

show abstract

“…Furthermore, the learning rules that models LTD in both classical conditioning and motor control are variations of functionally similar error correcting rules; compare, for instance, the learning rules for classical conditioning in ref. 42 and motor control in ref. 12.…”

Section: Discussionmentioning

confidence: 99%

Chaos may enhance information transmission in the inferior olive

Schweighofer

Doya

Fukai

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

120

View full text Add to dashboard Cite

Despite unique well characterized neuronal properties, such as extensive electrical coupling and low firing rates, the role of the inferior olive (IO), which is the source of the climbing fiber inputs to cerebellar Purkinje cells, is still controversial. We propose that the IO stochastically recodes the high-frequency information carried by its synaptic inputs into stochastic, low-rate spikes in its climbing fiber output. Computer simulations of realistic IO networks showed that moderate electrical coupling produced chaotic firing, which maximized the input-output mutual information. This ''chaotic resonance'' may allow rich error signals to reach individual Purkinje cells, even at low firing rates, allowing efficient cerebellar learning.O ver a century of cerebellar research has provided us with comprehensive understandings of cerebellar anatomy and physiology. It is well known, for instance, that the output neurons of the cerebellar cortex, the Purkinje cells, receive two major types of synaptic inputs: Ͼ100,000 parallel fibers and a single climbing fiber, an axon from an inferior olive (IO) neuron; whereas summation of parallel fiber inputs generate ''simple spikes,'' a single IO spike generates a ''complex spike'' through the powerful climbing fiber input. Furthermore, the major anatomical and electrophysiological properties of the IO neurons are well characterized (1). First, these neurons generate dendritic and somatic spikes at low firing rates in vivo (three spikes per sec at most) (2). Second, they are electrotonically coupled by gap junctions (3), more extensively than any other cells of the mammalian brain (4). Third, they exhibit subthreshold oscillations in vitro (5, 6). However, despite this detailed knowledge, we still lack a clear understanding of the function of the cerebellum, and two seemingly contradictory major hypotheses have been proposed, each based on a dramatically different view of the IO (7,8).According to the cerebellar learning hypothesis (9-13), when conjointly activated with parallel fibers, IO spikes modify cerebellar input-output transformations, in agreement with the known long-term depression (LTD) at the parallel fiberPurkinje cell synapse (14). Recent cerebellar motor learning theories (12, 15-19) make two further postulates relevant to this hypothesis. First, the IO neurons must fire at a low firing rate so that complex spikes encoding error signals do not interfere with simple spikes carrying motor control commands (12, 15). Second, the IO must transmit error signals (15, 20) with hightemporal resolution for cerebellar learning for efficient motor control.Alternatively, the cerebellar timing hypothesis states that the IO exerts its influence on motor control in real time via synchronous and rhythmic discharges (21). This hypothesis is in agreement with the facts that IO neurons are extensively electrically coupled via gap junctions (8) and that IO neurons fire with some degree of rhythmicity and pair-wise synchrony both in vitro (22) and in vivo (21). It is further support...

show abstract

“…The relation between the input signal and NM movement can be approximated by first-order differential equation (15), identical in form to that linking the firing of ocular motoneurons to rotatory eye movement (Keller 1981) under restricted conditions (Sklavos et al 2005). Could such an input signal be generated in a straightforward manner by appropriate increases in the firing rates of the neurons in the interpositus nucleus as assumed in many models of eyeblink conditioning (Balkenius and Morén 1999;Fiala et al 1996;Garenne and Chauvet 2004;Gluck et al 2001;Hofstötter et al 2002;Medina and Mauk 2000;Moore and Choi 1997)?…”

Section: Nature Of Control Signalmentioning

confidence: 99%

“…Initial data from multiunit recordings in the interpositus nucleus (McCormick and Thompson 1984) indicated a firing rate profile that simply mimicked the profile of the conditioned NMR. Consequently, many models of the cerebellum in eyeblink conditioning essentially stop at the interpositus nucleus, with no representation either of efferent target neural populations such as the red nucleus and motor nuclei, or of the plant itself (Balkenius and Morén 1999;Fiala et al 1996;Garenne and Chauvet 2004;Gluck et al 2001;Hofstötter et al 2002;Medina and Mauk 2000;Moore and Choi 1997). (The term plant refers to "that which is controlled," in this case by the signal sent from the motoneurons, and corresponds to the relevant muscles together with orbital or eyelid tissue).…”

Section: Introductionmentioning

confidence: 99%

Evidence From Retractor Bulbi EMG for Linearized Motor Control of Conditioned Nictitating Membrane Responses

Lepora¹,

Mavritsaki²,

Porrill³

et al. 2007

Journal of Neurophysiology

View full text Add to dashboard Cite

Lepora NF, Mavritsaki E, Porrill J, Yeo CH, Evinger C, Dean P. Evidence from retractor bulbi EMG for linearized motor control of conditioned nictitating membrane responses. J Neurophysiol 98: 2074 -2088, 2007. First published July 5, 2007 doi:10.1152/jn.00210.2007. Classical conditioning of nictitating membrane (NM) responses in rabbits is a robust model learning system, and experimental evidence indicates that conditioned responses (CRs) are controlled by the cerebellum. It is unknown whether cerebellar control signals deal directly with the complex nonlinearities of the plant (blinkrelated muscles and peripheral tissues) or whether the plant is linearized to ensure a simple relation between cerebellar neuronal firing and CR profile. To study this question, the retractor bulbi muscle EMG was recorded with implanted electrodes during NM conditioning. Pooled activity in accessory abducens motoneurons was estimated from spike trains extracted from the EMG traces, and its temporal profile was found to have an approximately Gaussian shape with peak amplitude linearly related to CR amplitude. The relation between motoneuron activity and CR profiles was accurately fitted by a first-order linear filter, with each spike input producing an exponentially decaying impulse response with time constant of order 0.1 s. Application of this first-order plant model to CR data from other laboratories suggested that, in these cases also, motoneuron activity had a Gaussian profile, with time-of-peak close to unconditioned stimulus (US) onset and SD proportional to the interval between conditioned stimulus and US onsets. These results suggest that for conditioned NM responses the cerebellum is presented with a simplified "virtual" plant that is a linearized version of the underlying nonlinear biological system. Analysis of a detailed plant model suggests that one method for linearising the plant would be appropriate recruitment of motor units.

show abstract

Cerebellar Substrates for Error Correction in Motor Conditioning

Cited by 43 publications

References 67 publications

Opioid Receptors in the Midbrain Periaqueductal Gray Regulate Extinction of Pavlovian Fear Conditioning

Opioid Receptors in the Midbrain Periaqueductal Gray Regulate Extinction of Pavlovian Fear Conditioning

Chaos may enhance information transmission in the inferior olive

Evidence From Retractor Bulbi EMG for Linearized Motor Control of Conditioned Nictitating Membrane Responses

Contact Info

Product

Resources

About