Fornix fibers and motivational states as controllers of behavior: A study stimulated by the contextual retrieval theory

doi:10.1016/S0091-6773(78)92583-X

Behavioral Biology

Volume 22, Issue 4, April 1978, Pages 463-478

https://doi.org/10.1016/S0091-6773(78)92583-X Get rights and content

The influence of medial septal lesions and total fornix transection upon the selection of learned responses by motivational states was examined. In one condition rats made hungry or thirsty on alternate days had to learn to turn one way for food and the opposite way for water in the same T-maze. Animals with similar lesions were run in another, two-maze, condition, which matched the single-maze condition in all respects except that food and water were available in separate mazes which in some respects were similar to each other and in others were different. The response tendencies (left vs right) during the early stages of learning were tabulated. When considered as individuals, lesioned animals displayed significantly more response bias than sham-operated controls. Correlations between the number of correct trials per session for obtaining food and that for obtaining water as learning proceeded were highly negative for the fornix-transection group in the single-maze condition; the same correlations for controls were low. In the single-maze condition animals with medial septal lesions reached the criterion more readily than controls, while those with fornix transections learned more slowly. No differences in trials to criterion were observed in the two-maze condition. Together the results are interpreted as indicating that these lesions alter the mode by which the information within motivational states selects learned responses for performance. This alteration can be predicted from the theory that the hippocampus is involved in contextual retrieval.

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This finding is consistent with our earlier report in healthy humans using a similar methodology to here (Dudley & Stevenson, 2016) – though noting this study did not find a correlation with cardiac interoception – to clinical findings from patients with lesions to the MTL (Berriman et al., 2016; Hebben et al., 1985; Higgs et al., 2008; Rozin et al., 1998), and to network imaging studies that find hippocampal involvement for several interoceptive tasks including cardiac interoception (Jarrahi et al., 2015; Kuehn et al., 2016; Ploghaus et al., 2001). It is also consistent with the animal literature that indicates that selective hippocampal lesions cause impairments in the ability of rats to utilise interoceptive cues to solve particular problems (Davidson & Jarrard, 1993; Davidson et al., 2010; Hirsh et al., 1978). While this growing body of findings indicates the importance of the hippocampus in interoceptive processing, and with a broad role at that (i.e., not just restricted to hunger and fullness), a key question remains; what is its function?
The hippocampus is involved in interoceptive processing (i.e., perceiving internal bodily states), with much of this evidence relating to hunger and fullness. Here we examine whether cardiac and self-report measures of interoception are related to two measures of hippocampal dependent learning and memory (HDLM) – the Rey Auditory Verbal Learning Test (RAVLT) and Logical Memory. Healthy adults completed a neuropsychological test battery including all of these measures, along with assessments of intelligence and executive function. Biographical, medical and psychological-related data that might confound detecting an HDLM-interoception relationship was also collected. Both measures of HDLM were associated with cardiac interoception after controlling for confounding variables. More accurate cardiac interoception was linked to better HDLM performance. On the self-report measure of interoception, better performance on the RAVLT was associated with better-reported attention regulation, consistent with the hippocampus’s known role in mindfulness. Overall, these findings suggest hippocampal involvement in cardiac and self-report interoceptive capacity. The broader functional role of the hippocampus in interoception is discussed.
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As noted above, different deprivation states can be seen as contexts that serve to retrieve or inhibit retrieval of associations between external cues and the US. More direct evidence for such a hippocampal-dependent contextual retrieval function was provided by [80], who showed that without the hippocampus rats were unable to use hunger and thirst cues to retrieve the memory of the locations of food and water (also see Hirsh et al. [64]). Furthermore, following recovery from surgery, rats with hippocampal lesions gain more weight than sham-lesioned controls [29,119].
Women are disproportionately affected by obesity, and obesity increases women's risk of developing dementia more so than men. Remarkably little is known about how females make decisions about when and how much to eat. Research in animal models with males supports a framework in which previous experiences with external food cues and internal physiological energy states, and the ability to retrieve memories of the consequences of eating, determines subsequent food intake. Additional evidence indicates that consumption of a high-fat, high-sugar diet interferes with hippocampal-dependent mnemonic processes that operate to suppress eating, such as in situations of satiety. Recent findings also indicate that weakening this form of hippocampal-dependent inhibitory control may also extend to other forms of learning and memory, perpetuating a vicious cycle of increased Western diet intake, hippocampal dysfunction, and further impairments in the suppression of appetitive behavior that may ultimately disrupt other types of memorial interference resolution. How these basic learning and memory processes operate in females to guide food intake has received little attention. Ovarian hormones appear to protect females from obesity and metabolic impairments, as well as modulate learning and memory processes, but little is known about how these hormones modulate learned appetitive behavior. Even less is known about how a sex-specific environmental factor – widespread hormonal contraceptive use – affects associative learning and the regulation of food intake. Extending learned models of food intake to females will require considerably investigation at many levels (e.g., reproductive status, hormonal compound, parity). This work could yield critical insights into the etiology of obesity, and its concomitant cognitive impairment, for both sexes.
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The anterior medial temporal lobes are one of the most studied parts of the brain. Classically, their two main structures – the amygdalae and the hippocampi – have been linked to key cognitive and affective functions, related in particular to learning and memory. Based on abundant evidence, we will argue for an alternative but complementary point of view: they may also play a major role in food intake and body weight regulation. First, an overview is given of early clinical evidence in this line of thought. Subsequently, empirical evidence is presented on how food intake, including in the extreme case of obesity, may relate to amygdalian and hippocampal functioning. The focus is on the amygdala's role in processing the relevance of food stimuli, cue-induced feeding, and stress-induced eating and on the hippocampus' involvement in the use of interoceptive signals of hunger and satiety, as well as memory and inhibitory processes related to food intake. Additionally, an elaboration takes place on possible reciprocal links between food intake, body weight, and amygdala and hippocampus functioning. Finally, issues that seemed particularly critical for future research in the field are discussed.
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Although these are novel findings, as no study has previously tested for these types of association in healthy adult participants before, we suggest that they are to be expected. The well-established animal lesion evidence indicates a role for the hippocampus in interoception (Clifton et al., 1998; Davidson & Jarrard, 1993; Hirsh et al., 1978; Hsiao & Isaacson, 1971). Similarly the human neuropsychological literature suggests that medial temporal lobe structures play a role in interoceptive awareness (Hebben et al., 1985; Rozin et al., 1998), as does the ingestion-related neuroimaging data (e.g., DelParigi et al., 2004).
Many neuropsychological and animal lesion studies point to the hippocampus as being critical for mediating interoceptive awareness, while neuroimaging studies have been used to argue for the importance of the insula and anterior cingulate cortex. Here, using healthy young adults – as with the neuroimaging data – we tested for an association between performance on a hippocampal dependent learning and memory (HDLM) measure (logical memory percent retention) and interoceptive awareness assessed on three tasks – heart rate tracking, water loading and the Multidimensional Assessment of Interoceptive Awareness questionnaire (MAIA). After controlling for other relevant potentially confounding variables, we found significant associations between both the water loading and MAIA measures (which were both correlated) and HDLM performance. These findings imply that hippocampal dependent processes are involved in interoceptive awareness in healthy young adults. More tentatively, they suggest that medial temporal lobe structures may mediate interoceptive tasks that involve ingestion and/or integration of past and current state-based information.
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Citation Excerpt :
A variety of evidence shows that consuming a Western-style diet can impair the performance of rodents and humans on learning and memory problems that depend on the functional integrity of the hippocampus [11–15]. Other studies in our laboratory and elsewhere have demonstrated that the ability to use interoceptive food deprivation and hydrational stimuli to solve discrimination problems is also dependent on the hippocampus [16–19]. In contrast, there is little evidence that the hippocampus is required to learn about simple nonspatial discriminative stimuli [20,21].
In obesogenic environments food-related external cues are thought to overwhelm internal cues that normally regulate energy intake. We investigated how this shift from external to internal stimulus control might occur. Experiment 1 showed that rats could use stimuli arising from 0 and 4 h food deprivation to predict sucrose delivery. Experiment 2 then examined (a) the ability of these deprivation cues to compete with external cues and (b) how consuming a Western-style diet (WD) affects that competition. Rats were trained to use both their deprivation cues and external cues as compound discriminative stimuli. Half of the rats were then placed on WD while the others remained on chow, and external cues were removed to assess learning about deprivation state cues. When tested with external cues removed, chow-fed rats continued to discriminate using only deprivation cues, while WD-fed rats did not. The WD-fed group performed similarly to control groups trained with a noncontingent relationship between deprivation cues and sucrose reinforcement. Previous studies provided evidence that discrimination based on interoceptive deprivation cues depends on the hippocampus and that WD intake could interfere with hippocampal functioning. A third experiment assessed the effects of neurotoxic hippocampal lesions on weight gain and on sensitivity to the appetite-suppressing effects of the satiety hormone cholecystokinin (CCK). Relative to controls, hippocampal-lesioned rats gained more weight and showed reduced sensitivity to a 1.0 ug but not 2.0 or 4.0 ug CCK doses. These findings suggest that WD intake reduces utilization of interoceptive energy state signals to regulate appetitive behavior via a mechanism that involves the hippocampus.

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¹: This work was supported by a grant from the National Research Council of Canada, No. A-7918, and a team grant from the Quebec Ministry of Education to Dr. D. Bindra. We would like to thank Drs. Peter Milner and Norman White for their counsel.

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Fornix fibers and motivational states as controllers of behavior: A study stimulated by the contextual retrieval theory1

Behav. Biol.

Physiol. Behav.

Physiol. Behav.