Neurotoxic Lesions of the Medial Mediodorsal Nucleus of the Thalamus Disrupt Reinforcer Devaluation Effects in Rhesus Monkeys

Mitchell, Anna S.; Browning, Philip J.; Baxter, Mark G.

doi:10.1523/jneurosci.1914-07.2007

Cited by 91 publications

(137 citation statements)

References 40 publications

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“…The results from multiple reinforcer Pavlovian devaluation tasks in these studies are consistent with the data in the macaque literature, with devaluation performance impaired by MD lesions in monkeys which have been previously exposed to different reward contingencies (Izquierdo & Murray, 2004b;Mitchell et al, 2007), although neither macaque experiment used an explicitly Pavlovian task prior to operant devaluation. The present data are in conflict, however, with those of Corbit and colleagues (2003), who found that naïve rats are impaired in a multiple reinforcer operant devaluation task.…”

Section: Discussionsupporting

confidence: 87%

“…There does not appear to be a simple dichotomy in which the first task a rat learns is sensitive to outcome devaluation regardless of whether MD is intact and all subsequent tasks are sensitive to devaluation only in rats with MD intact. It appears that there may be a requirement for a change in associative contingencies in order for MD to be required for devaluation.The results from multiple reinforcer Pavlovian devaluation tasks in these studies are consistent with the data in the macaque literature, with devaluation performance impaired by MD lesions in monkeys which have been previously exposed to different reward contingencies (Izquierdo & Murray, 2004b;Mitchell et al, 2007), although neither macaque experiment used an explicitly Pavlovian task prior to operant devaluation. The present data are in conflict, however, with those of Corbit and colleagues (2003), who found that naïve rats are impaired in a multiple reinforcer operant devaluation task.…”

supporting

confidence: 87%

“…MD lesions impair devaluation in operant devaluation tasks in rats (Corbit, Muir & Balleine, 2003) and macaques (Mitchell, Browning, & Baxter, 2007), and disconnections of MD from BLA and OFC impair the performance of macaques in an operant devaluation experiment (Izquierdo & Murray, 2004b).…”

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confidence: 99%

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A limited role for mediodorsal thalamus in devaluation tasks.

Pickens

2008

Behavioral Neuroscience

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Six experiments were performed to determine the role of mediodorsal thalamus (MD) in the devaluation task, varying the type of contingencies (Pavlovian or operant), the number of reinforcers (one versus two) and the order of experiments (in naïve or experimentally experienced rats). MD lesioned rats were impaired in devaluation performance when switched between Pavlovian and operant devaluation tasks, but not when switched from one Pavlovian devaluation task to another Pavlovian devaluation task. MD lesions caused no devaluation impairment in a multiple reinforcer Pavlovian devaluation task. These results suggest that MD lesions impair performance in devaluation tasks as a result of an inability to switch the form of associations made from one type of outcome-encoding association to another. This is in accord with previous literature suggesting that MD is needed for strategy set shifting. The results further suggest that MD is a necessary part of devaluation circuits only in cases in which previous associations need to be suppressed in order for new associations to be learned and control behavior, and otherwise the devaluation circuit does not require MD. KeywordsMediodorsal thalamus; devaluation; set-shifting; reward Devaluation tasks involve training a relationship that earns or predicts a valuable outcome, such as a lever press that earns a type of food or a light that predicts the delivery of food (Adams & Dickinson, 1981;Holland & Rescorla, 1975). The value of this outcome is then reduced by motivational (e.g., satiation) or associative methods (e.g., a food aversion is established by food-toxin pairings). After such outcome devaluation, responding based on the relationship that predicts or earns food is typically reduced. Similarities in task demands to human decision making, as well as similarities in neural underpinnings, suggests that the devaluation task provides a model of goal expectancy-guided behavior (as reviewed in Pickens & Holland, 2004).Many reports have examined the neural circuitry involved in acting according to the current value of goals. For example, lesions of amygdala, or specific lesions of basolateral complex of amygdala (BLA), cause impairments in many versions of the devaluation task (Balleine, Killcross, & Dickinson, 2003;Blundell, Hall & Killcross, 2003;Hatfield, Han, Conley, Gallagher, & Holland, 1996;Malkova, Gaffan & Murray, 1997). Several laboratories have also found that bilateral orbitofrontal cortex (OFC) lesions (Gallagher, McMahan & Schoenbaum, 1999;Izquierdo, Suda & Murray, 2004; but see Ostlund & Balleine, 2007) or lesions that disconnect amygdala and OFC (Baxter, Parker, Lindner, Izquierdo, & Murray, 2000) impair performance in devaluation tasks. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptAnother brain area that may be needed for devaluation is mediodorsal thalamus (MD). MD, BLA and OFC are all interconnected (Carmichael & Price, 1995;Ghashghaei & Barbas, 2002;Groenewegen, 1988;Ray & Price, 1992) and the three brain areas share s...

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Section: Discussionsupporting

confidence: 87%

supporting

confidence: 87%

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A limited role for mediodorsal thalamus in devaluation tasks.

Pickens

2008

Behavioral Neuroscience

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“…There was inconsistent evidence of a delay-dependent impairment (Mumby et al 1993). The results suggest that a major effect of medial dorsal lesions is not on object recognition per se but rather on other aspects of task acquisition and performance, such as sensitivity to the reinforcement contingency (McAlonan et al 1993;Mitchell et al 2007).…”

Section: Medial Dorsal Thalamic Nucleusmentioning

confidence: 84%

Unraveling the contributions of the diencephalon to recognition memory: A review

Aggleton¹,

Dumont²,

Warburton³

2011

Learn. Mem.

137

111

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Both clinical investigations and studies with animals reveal nuclei within the diencephalon that are vital for recognition memory (the judgment of prior occurrence). This review seeks to identify these nuclei and to consider why they might be important for recognition memory. Despite the lack of clinical cases with circumscribed pathology within the diencephalon and apparent species differences, convergent evidence from a variety of sources implicates a subgroup of medial diencephalic nuclei. It is supposed that the key functional interactions of this subgroup of diencephalic nuclei are with the medial temporal lobe, the prefrontal cortex, and with cingulate regions. In addition, some of the clinical evidence most readily supports dual-process models of recognition, which assume two independent cognitive processes (recollective-based and familiarity-based) that combine to direct recognition judgments. From this array of information a "multi-effect multinuclei" model is proposed, in which the mammillary bodies and the anterior thalamic nuclei are of preeminent importance for recollective-based recognition. The medial dorsal thalamic nucleus is thought to contribute to familiarity-based recognition, but this nucleus, along with various midline and intralaminar thalamic nuclei, is also assumed to have broader, indirect effects upon both recollective-based and familiarity-based recognition.Clinical studies repeatedly show that diencephalic pathology can impair recognition memory. Even so, there is no agreed locus within the diencephalon responsible for this memory loss and, hence, no agreed mechanism to explain the impairment. The present review examines both clinical and animal findings, and from this information a multi-effect multi-nuclei (MEMN) model emerges to explain the contributions of the diencephalon to recognition memory.At the outset, it is necessary to refine the focus of this review and to define some of its principal terms. The diencephalon comprises the thalamus and hypothalamus but, as will be explained, only the more medial parts of the diencephalon will be considered in detail. Recognition memory refers to the ability to detect whether a stimulus (e.g., a word, face, picture, object, or sound) has previously been encountered. As a consequence, this review is not about item identification (sometimes also confusingly referred to as recognition). Likewise, conditions that have broad disruptive effects on cognition, e.g., dementia, will not be considered even though recognition is typically impaired. Distinctions will be made between "item recognition," where the task is to determine if an individual item is novel or familiar, and "associative recognition," where all the individual items being experienced are familiar, but their particular combination is novel. A further, distinct ability is "recency" discrimination-the ability to determine which of two familiar stimuli has been experienced more recently. Both studies of amnesia and electrophysiological recordings show how recency memory and recogniti...

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“…A more detailed description of the surgical methods and preoperative and postoperative drug treatments was provided by Mitchell et al (2007a). Briefly, each monkey was sedated on the morning of surgery with both ketamine and xylazine and then intubated and, during surgery, was mechanically ventilated and maintained deeply anesthetized using both gaseous [sevoflurane (1.4 -3.0%, to effect, in 100% oxygen)] and intravenous [alfentanil (0.5-3.0 g/kg)] anesthesia.…”

Section: Surgical Proceduresmentioning

confidence: 99%

Dissociable Roles for Cortical and Subcortical Structures in Memory Retrieval and Acquisition

Mitchell

Browning²,

Wilson³

et al. 2008

J. Neurosci.

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The relationship between anterograde and retrograde amnesia remains unclear. Previous data from both clinical neuropsychology and monkey lesion studies suggest that damage to discrete subcortical structures leads to a relatively greater degree of anterograde than retrograde amnesia, whereas damage to discrete regions of cortex leads to the opposite pattern of impairments. Nevertheless, damage to the medial diencephalon in humans is associated with both retrograde and anterograde amnesia. In the present study, we sought to reconcile this by assessing retention as well as subsequent relearning and new postoperative learning. Rhesus monkeys learned 300 unique scene discriminations preoperatively, and retention was assessed in a preoperative and postoperative one-trial retrieval test. Combined bilateral subcortical lesions to the magnocellular mediodorsal thalamus and fornix impaired postoperative retention of the preoperatively acquired information. In addition, subsequent relearning and new postoperative learning were also impaired. This contrasts with the effects of a discrete lesion to just one of these structures, after which retention is intact in both cases. Discrete bilateral ablations to the entorhinal cortex impaired retention but had no effect on new learning. Combined with previous work from our laboratory, these results support the hypothesis that subcortical damage has a relatively greater effect on new learning, and cortical damage has a relatively greater effect on retention. Furthermore, the results demonstrate that retrograde amnesia occurs as a result of subcortical damage only if it is widespread, leading to an extensive disruption of cortical functioning. Damage of this nature may account for dense amnesia.

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Neurotoxic Lesions of the Medial Mediodorsal Nucleus of the Thalamus Disrupt Reinforcer Devaluation Effects in Rhesus Monkeys

Cited by 91 publications

References 40 publications

A limited role for mediodorsal thalamus in devaluation tasks.

A limited role for mediodorsal thalamus in devaluation tasks.

Unraveling the contributions of the diencephalon to recognition memory: A review

Dissociable Roles for Cortical and Subcortical Structures in Memory Retrieval and Acquisition

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