Rapid forgetting of individual spatial reversal problems in rats with parafascicular lesions

Thompson, Robert; Kao, Lisa; Yang, Solomon

doi:10.1016/s0163-1047(81)92189-0

Cited by 26 publications

(11 citation statements)

References 27 publications

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“…Pf inactivation did not affect place acquisition, but impaired place reversal learning. The reversal learning deficit observed following Pf inactivation is consistent with results indicating that posterior intralaminar thalamic lesions, that include the Pf, do not impair acquisition of various discrimination tests (Nyakas et al, 1985; Quiroz-Padilla et al, 2007; Savage et al, 1997), but do impair reversal learning (Nyakas et al, 1985; Thompson et al, 1981). In past experiments, lesions extended beyond the Pf and damaged fibers of passage.…”

Section: Discussionsupporting

confidence: 87%

The Parafascicular Thalamic Nucleus Concomitantly Influences Behavioral Flexibility and Dorsomedial Striatal Acetylcholine Output in Rats

Brown¹,

Baker²,

Ragozzino³

2010

J. Neurosci.

124

134

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Recent evidence suggests that a circuit involving the centromedian-parafascicular (Pf) thalamus and basal ganglia is critical for a shift away from biased actions. In particular, excitatory input from the Pf onto striatal cholinergic neurons may facilitate behavioral flexibility. Accumulating evidence indicates that an endogenous increase in dorsomedial striatal acetylcholine (ACh) output enhances behavioral flexibility. The present experiments investigated whether the rat (Rattus norvegicus) Pf supports flexibility during reversal learning, in part, by modifying dorsomedial striatal ACh output. This was determined first by examining the effects of Pf inactivation, through infusion of the GABA agonists baclofen and muscimol, on place acquisition and reversal learning. Additional experiments examined Pf inactivation on dorsomedial striatal ACh output during reversal learning and a resting condition. Behavioral testing was performed in a cross-maze. In vivo microdialysis combined with HPLC/electrochemical detection was used to sample ACh from the dorsomedial striatum. Pf inactivation selectively impaired reversal learning in a dose-dependent manner. A subsequent study showed that an increase in dorsomedial striatal ACh efflux (ϳ30% above basal levels) during reversal learning was blocked by Pf inactivation, which concomitantly impaired reversal learning. In the resting condition, a dose of baclofen and muscimol that blocked a behaviorally induced increase in dorsomedial striatal ACh output did not reduce basal ACh efflux. Together, the present findings indicate that the Pf is an intralaminar thalamic nucleus critical for behavioral flexibility, in part, by directly affecting striatal ACh output under conditions that require a shift in choice patterns.

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Section: Discussionsupporting

confidence: 87%

The Parafascicular Thalamic Nucleus Concomitantly Influences Behavioral Flexibility and Dorsomedial Striatal Acetylcholine Output in Rats

Brown¹,

Baker²,

Ragozzino³

2010

J. Neurosci.

124

134

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“…However, the Huppert and Piercy proposal that diencephalic lesions are associated with learning defects alone and that retention defects alone or in combination with learning defects arise only from hippocampal lesions may not apply to lower mammalian forms to the same extent that it applies to amnesic patients. For example, rats with parafascicular thalamic lesions have been observed to show defects in both learning and retention of individual spatial reversal problems (Thompson, Kao, & Yang, 1981). Similar findings have been reported in rats with lesions to either the rostral caudoputamen or substantia nigra (Thompson & Yang, 1982).…”

mentioning

confidence: 63%

“…The criterion of learning was defined as the first appearance of a "perfect" (Grant, 1946) or "nearperfect" (Runnels, Thompson, & Runnels, 1968) run of correct responses having a probability of occurrence of less than .OS. (This type of criterion is particularly suitable when investigating retentiveness of a habit in two or more groups of subjects that differ significantly from each other in the rate of originallearning-see Thompson et al, 1981).…”

Section: Methodsmentioning

confidence: 99%

Abnormal learning and forgetting of individual spatial reversal problems in brain-damaged rats

Thompson

1983

Psychobiology

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Except for amygdaloid lesions and cortical cerebellar ablations, selective destruction of virtually any part of the tel-, di-, mes-, or metencephalon was found to impede spatial reversal learning in the rat. (These data contrast sharply with those reported in recent studies on visual reversal learning in the rat.) Test trials given after learning each reversal problem disclosed significant (or marginally significant) deficits in retention only in those groups sustaining damage to the cingulate cortex, ventral hippocampus, rostral caudoputamen, lateral supraoptic hypothalamus, posterolateral hypothalamus, lateral thalamic complex, mediodorsal thalamus, ventromedial thalamus, parafascicular nucleus, substantia nigra, interpeduncular-central tegmental area, pontomesencephalic reticular formation, or pontine reticular formation. It is proposed that there may be at least three classes of learning (amnesic) disorders observed on any given task: (1) a learning impairment only, (2) a retention impairment only, and (3) both a learning and retention impairment.Huppert and Piercy (1979) have presented evidence suggesting that there may be at least two classes of learning (amnesic) disorders in braindamaged patients. In one, learning is impaired, but retention over time of what has been learned is unimpaired. The second is characterized by an impairment (or no impairment) in learning, but retention over time of what has been learned is impaired.

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“…The marked anatomical differences observed in the distribution of thalamostriatal projections in Ten-m3 KO mice suggested the possibility of behavioral consequences. Because we were unable to test Ten-m3 KOs for complex goal-directed learning (see Discussion), functions best linked to this pathway (Thompson et al, 1981;Matsumoto et al, 2001;Kato et al, 2011;Bradfield et al, 2013), we adopted a non-visual, striatally dependent motor skill/procedural learning paradigm using an accelerating rotorod. Changes in the animals' abilities to stay on the apparatus were examined over multiple sessions to allow for the comparison of na€ ıve motor performance (i.e.…”

Section: Ten-m3 Kos Exhibit Deficits In Motor Skill Acquisitionmentioning

confidence: 99%

“…Likewise, both the striatum and thalamus are implicated in procedural learning (Kumari et al, 2002;Hubert et al, 2007). In rodents, these pathways are critically involved in the regulation of goal-directed learning and behavioral flexibility (Thompson et al, 1981;Ragozzino, 2004;Bradfield et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

The glycoprotein Ten‐m3 mediates topography and patterning of thalamostriatal projections from the parafascicular nucleus in mice

Tran

Sawatari

Leamey

2014

Eur J of Neuroscience

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The striatum is the key input nucleus of the basal ganglia, and is implicated in motor control and learning. Despite the importance of striatal circuits, the mechanisms associated with their development are not well established. Previously, Ten-m3, a member of the Ten-m/teneurin/odz family of transmembrane glycoproteins, was found to be important in the mapping of binocular visual pathways. Here, we investigated a potential role for Ten-m3 in striatal circuit formation. In situ hybridisation revealed a patchy distribution of Ten-m3 mRNA expression superimposed on a high-dorsal to low-ventral gradient in a subregion of the striatal matrix. A survey of afferent/efferent structures associated with the matrix identified the parafascicular thalamic nucleus (PF) as a potential locus of action. Ten-m3 was also found to be expressed in a high-dorsal to low-ventral gradient in the PF, corresponding topographically to its expression in the striatum. Further, a subset of thalamic terminal clusters overlapped with Ten-m3-positive domains within the striatal matrix. Studies in wild-type (WT) and Ten-m3 knockout (KO) mice revealed no differences in overall striatal or PF structure. Thalamostriatal terminals in KOs, however, while still confined to the matrix subregion, lost their clustered appearance. Topography was also altered, with terminals from the lateral PF projecting ectopically to ventral and medial striatum, rather than remaining confined dorsolaterally as in WTs. Behaviorally, Ten-m3 KOs displayed delayed motor skill acquisition. This study demonstrates that Ten-m3 plays a key role in directing the formation of thalamostriatal circuitry, the first molecular candidate reported to regulate connectivity within this pathway.

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Rapid forgetting of individual spatial reversal problems in rats with parafascicular lesions

Cited by 26 publications

References 27 publications

The Parafascicular Thalamic Nucleus Concomitantly Influences Behavioral Flexibility and Dorsomedial Striatal Acetylcholine Output in Rats

The Parafascicular Thalamic Nucleus Concomitantly Influences Behavioral Flexibility and Dorsomedial Striatal Acetylcholine Output in Rats

Abnormal learning and forgetting of individual spatial reversal problems in brain-damaged rats

The glycoprotein Ten‐m3 mediates topography and patterning of thalamostriatal projections from the parafascicular nucleus in mice

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