Effects of ipsilateral rostral pontine reticular lesions on retention of classically conditioned nictitating membrane and eyelid responses

Lavond, David G.; McCormick, David A.; Clark, Gregory A.; Holmes, David T.; Thompson, Richard F.

doi:10.3758/bf03326990

Cited by 72 publications

(34 citation statements)

References 14 publications

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“…Subsequent group analysis indicated that most sensitive sites were located within 0.5 mm of the rostral half of the medial dentate/lateral interpositus region, ranging within this structure from 0.5 to 1.5 mm rostral to lambda. These anatomical boundaries are consistent with the areas reported as the most effective sites for abolishing the CR in the lesion/ablation studies (1)(2)(3)(4)(5)(6)(7)(8)(9) used to determine the drug-dose relationship of these antagonists or the effects of bicuculline methiodide on the ipsilateral vs. contralateral NM response (study 1, 8 of 13 animals had such placements; study 2, 7 of 11 animals; and study 4, 4 of 7 animals). In contrast, the remaining animals with cannula placements in more posterior regions of the medial dentate/lateral interpositus region, as well as animals with cannula placements located more distal to the deep nuclei in the overlying white matter, displayed drug effects either less effective or totally ineffective in reducing the CR peak amplitude.…”

Section: Resultssupporting

confidence: 73%

“…Work in Thompson's laboratory (1)(2)(3)(4) initially demonstrated that discrete lesions of the medial dentate/lateral interpositus region, or the superior cerebellar peduncle, could selectively disrupt acquisition, retention, and relearning of this associative task. These observations were subsequently confirmed by others (5); the critical nuclear region appears to be the anterior lateral interpositus (6,7).…”

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confidence: 99%

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Cerebellar GABAergic processes: evidence for critical involvement in a form of simple associative learning in the rabbit.

Mamounas¹,

Thompson²,

Madden³

1987

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

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Converging evidence from electrophysiological recording and lesion studies suggests an essential role for the cerebellum in classical conditioning of the nictitating membrane response in the rabbit. The present study begins to delineate within this structure neurotransmitter systems that appear critical for the expression of this form of simple associative learning. Experiments reported here demonstrate that microinfusion of y-aminobutyric acid (GABA) antagonists (either bicuculline methiodide or picrotoxin) into specific areas of the medial dentate/lateral interpositus nuclei or into the cerebellar cortex of lobule HVI can selectively and reversibly abolish conditioned responding, while leaving the unconditioned reflex response intact. The results are consistent with the suggestion that GABAergic synapses play an essential role in the circuitry that mediates the conditioned response.Experimental evidence suggests an essential role for the dentate/interpositus nuclei of the cerebellum in a form of simple associative learning, classical conditioning of the rabbit nictitating membrane (NM) response. Work in Thompson's laboratory (1-4) initially demonstrated that discrete lesions of the medial dentate/lateral interpositus region, or the superior cerebellar peduncle, could selectively disrupt acquisition, retention, and relearning of this associative task. These observations were subsequently confirmed by others (5); the critical nuclear region appears to be the anterior lateral interpositus (6, 7). Moreover, electrophysiological analysis revealed that training-induced modifications in neural activity, which precede and model the conditioned response, develop in this region and in localized regions of the cerebellar cortex during learning (8,9). These observations suggest that some neural modification critical for the acquisition and retention of this associative task may be located within the cerebellar circuitry (10).As a preliminary step in elucidating potential synaptic circuitry subserving classical conditioning of the NM response, a series of pharmacological studies was initiated. Such analysis not only circumvents the difficulties intrinsic to ablation/ lesion experimental approaches but also may provide an initial characterization of critical neurotransmitter systems. Noting that an extensive literature indicates that intrinsic cerebellar neurons appear to be predominantly GABAergic (11), these initial experimental manipulations were directed at determining whether microinfusion of y-aminobutyric acid (GABA) antagonists within select regions of the cerebellum could effect retention of this form of simple associative learning.MATERIALS AND METHODS Thirty-five male New Zealand albino rabbits (Oryctolagus cuniculus), weighing 2-3 kg at the beginning of the experiment, were used. Animals were individually housed with ad lib access to food and water.Surgical Procedures. Animals were anesthetized with Halothane, and a cannula/electrode assembly was implanted into either the left dentate/interpositus or fas...

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Section: Resultssupporting

confidence: 73%

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confidence: 99%

Cerebellar GABAergic processes: evidence for critical involvement in a form of simple associative learning in the rabbit.

Mamounas¹,

Thompson²,

Madden³

1987

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

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“…Results of previous studies in our laboratory support the hypoth esis that the esse ntial mem ory trace(s) for eyelid conditioning and learn ing of other discrete behavioral respon ses are estab lished in the cerebellum and lor in struc tures afferent to the cerebellum for which the cerebellum is a mandatory efferent (e.g., Clark, McCormick, Lavond , & Thompson , 1984;Lavond, McCormick, Clark, Holmes, & Thompson, 1981;Lavond , McCormi ck, & Thompson, 1984;McCorm ick et aI., 1982 ;McC ormi ck et aI., 1981;McC ormick & Thompson, 1984a, 1984bThompson et al ., 1984). The pre sent result, that acti vation of mossy fiber proje cti ons to the cerebellum is an effe ctive CS , together with our results indicating that the climbing fiber projection from the inferior olive appears to be the necessary and sufficient "teaching " or " reinforcing" input McC ormick et al, in press;Steinmetz et al, 1984) support the hypothe sis that essent ial memory traces are establi shed in the ce rebellum.…”

Section: Discussionsupporting

confidence: 65%

Classical conditioning of the rabbit eyelid response with mossy fiber stimulation as the conditioned stimulus

Steinmetz

Lavond

Thompson

1985

Bull. Psychon. Soc.

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The nictitating membrane responses of 12 rabbits were classically conditioned using mossy fiber stimulation as a conditioned stimulus (CS) and airpuff as an unconditioned stimulus. The dorsolateral pontine nucleus and the lateral reticular nucleus were effective stimulation-CS sites for learning. Robust conditioned responses were obtained with relatively few paired trials and extinguished with subsequent CS-alone presentations. In addition, explicitly unpaired presentations of stimulation and airpufffailed to produce response increments. These results support previous theories of cerebellar function that have proposed that mossy fibers supply " learning" input to the cerebellum for motor learning.

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“…Electrophysiological data indicate that stimulus-evoked responses occur in the pons to both light-and tone-conditioned stimuli, as well as learning-related "models" that are increases in unit activity correlated to the rabbit eye-blink behavior or conditioned response (Steinmetz et al 1987;McCormick et al 1983). There is also some evidence that the pontine nuclei receive unconditioned stimulus somatosensory information (Lavond et al 1981;McCormick et al 1983). These anatomical and electrophysiological findings suggest that the pons could be a site of convergence of conditioned stimulus and unconditioned stimulus information, and therefore, could possibly be a locus of essential association for the learned response.…”

Section: Introductionmentioning

confidence: 88%

The effects of reversible inactivation of the red nucleus on learning-related and auditory-evoked unit activity in the pontine nuclei of classically conditioned rabbits.

Cartford

Gohl²,

Singson³

et al. 1997

Learn. Mem.

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The pontine nuclei carry auditory conditioned stimulus information to the cerebellum during classical conditioning of the nictitating membrane response in rabbits. In well-trained animals learning-related as well as stimulus-evoked unit activity can be recorded throughout the pontine nuclei but particularly in the lateral and dorsolateral pons. Recent work in our laboratory has provided evidence that the learning-related unit activity in the pons is dependent on the interpositus nucleus and that the pons is not a site of essential plasticity for the learned response. In the present study we considered the question of whether learning-related unit activity might be projected from the interpositus nucleus to the pons through the red nucleus, a primary output target of the interpositus and a structure known to be essential for expression of the learned response. Multiple unit recordings were taken from lateral and dorsolateral pontine locations in well-trained rabbits before and during cooling of the red nucleus. Analysis of pooled data for all recording locations within the lateral and dorsolateral pons indicated that reversible inactivation of red nucleus abolished both stimulus-evoked and learning-related unit activity. However, we also found discrete recording locations where stimulus-evoked and learning-related 1Corresponding author. unit activity were attenuated but not abolished by red nucleus cooling.

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Effects of ipsilateral rostral pontine reticular lesions on retention of classically conditioned nictitating membrane and eyelid responses

Cited by 72 publications

References 14 publications

Cerebellar GABAergic processes: evidence for critical involvement in a form of simple associative learning in the rabbit.

Cerebellar GABAergic processes: evidence for critical involvement in a form of simple associative learning in the rabbit.

Classical conditioning of the rabbit eyelid response with mossy fiber stimulation as the conditioned stimulus

The effects of reversible inactivation of the red nucleus on learning-related and auditory-evoked unit activity in the pontine nuclei of classically conditioned rabbits.

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