scholarly journals Lesion of striatal patches disrupts habitual behaviors and increases behavioral variability

2019 ◽  
Author(s):  
Jacob A. Nadel ◽  
Maya Neidhart ◽  
Sean S. Pawelko ◽  
Della Copes-Finke ◽  
Christopher D. Howard

AbstractHabits are automated behaviors that are insensitive to changes in behavioral outcomes. Habitual responding is thought to be mediated by striatum, with medial striatum guiding goal-directed action and lateral striatum promoting habits. However, interspersed throughout the striatum are neurochemically differing subcompartments known as patches, which are characterized by distinct molecular profiles relative to the surrounding matrix tissue. These structures have been thoroughly characterized neurochemically and anatomically, but little is known regarding their function. Patches have been shown to be selectively activated during inflexible motor stereotypies elicited by stimulants, suggesting that patches may subserve habitual behaviors. To explore this possibility, we utilized transgenic mice (Sepw1 NP67) expressing Cre recombinase in striatal patches to target these neurons for selective ablation with a virus driving Cre-dependent expression of caspase 3. Mice were then trained to press a lever for sucrose rewards on a variable interval schedule to elicit habitual responding. Mice were not impaired on the acquisition of this task, but lesioning striatal patches disrupted behavioral stability across training and lesioned mice utilized a more goal-directed behavioral strategy during training. Similarly, when mice were forced to omit responses to receive sucrose rewards, habitual responding was impaired in lesioned mice. To rule out effects of lesion on motor behaviors, mice were then tested for impairments in motor learning on a rotarod and locomotion in an open field. We found that patch lesions specifically impaired initial performance on the rotarod without modifying locomotor behaviors in open field. This work indicates that patches promote behavioral stability and habitual responding, adding to a growing literature implicating striatal patches in stimulus-response behaviors.

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
J. A. Nadel ◽  
S. S. Pawelko ◽  
J. R. Scott ◽  
R. McLaughlin ◽  
M. Fox ◽  
...  

AbstractHabits are inflexible behaviors that develop after extensive repetition, and overreliance on habits is a hallmark of many pathological states. The striatum is involved in the transition from flexible to inflexible responding, and interspersed throughout the striatum are patches, or striosomes, which make up ~15% of the volume of the striatum relative to the surrounding matrix compartment. Previous studies have suggested that patches are necessary for normal habit formation, but it remains unknown exactly how patches contribute to habit formation and expression. Here, using optogenetics, we stimulated striatal patches in Sepw1-NP67 mice during variable interval training (VI60), which is used to establish habitual responding. We found that activation of patches at reward retrieval resulted in elevated responding during VI60 training by modifying the pattern of head entry and pressing. Further, this optogenetic manipulation reduced subsequent responding following reinforcer devaluation, suggesting modified habit formation. However, patch stimulation did not generally increase extinction rates during a subsequent extinction probe, but did result in a small ‘extinction burst’, further suggesting goal-directed behavior. On the other hand, this manipulation had no effect in omission trials, where mice had to withhold responses to obtain rewards. Finally, we utilized fast-scan cyclic voltammetry to investigate how patch activation modifies evoked striatal dopamine release and found that optogenetic activation of patch projections to the substantia nigra pars compacta (SNc) is sufficient to suppress dopamine release in the dorsal striatum. Overall, this work provides novel insight into the role of the patch compartment in habit formation, and provides a potential mechanism for how patches modify habitual behavior by exerting control over dopamine signaling.


2016 ◽  
Vol 28 (7) ◽  
pp. 1024-1038 ◽  
Author(s):  
Theresa H. McKim ◽  
Daniel J. Bauer ◽  
Charlotte A. Boettiger

Learned habitual responses to environmental stimuli allow efficient interaction with the environment, freeing cognitive resources for more demanding tasks. However, when the outcome of such actions is no longer a desired goal, established stimulus–response (S-R) associations or habits must be overcome. Among people with substance use disorders (SUDs), difficulty in overcoming habitual responses to stimuli associated with their addiction in favor of new, goal-directed behaviors contributes to relapse. Animal models of habit learning demonstrate that chronic self-administration of drugs of abuse promotes habitual responding beyond the domain of compulsive drug seeking. However, whether a similar propensity toward domain-general habitual responding occurs in humans with SUDs has remained unclear. To address this question, we used a visuomotor S-R learning and relearning task, the Hidden Association between Images Task, which employs abstract visual stimuli and manual responses. This task allows us to measure new S-R association learning and well-learned S-R association execution and includes a response contingency change manipulation to quantify the degree to which responding is habit-based, rather than goal-directed. We find that people with SUDs learn new S-R associations as well as healthy control participants do. Moreover, people with an SUD history slightly outperform controls in S-R execution. In contrast, people with SUDs are specifically impaired in overcoming well-learned S-R associations; those with SUDs make a significantly greater proportion of perseverative errors during well-learned S-R replacement, indicating the more habitual nature of their responses. Thus, with equivalent training and practice, people with SUDs appear to show enhanced domain-general habit formation.


2021 ◽  
Author(s):  
Valentina Glück ◽  
Katharina Zwosta ◽  
Uta Wolfensteller ◽  
Hannes Ruge ◽  
Andre Pittig

Avoidance habits potentially contribute to maintaining maladaptive, costly avoidance behaviors that persist in the absence of threat. However, experimental evidence about costly habitual avoidance is scarce. In two experiments, we tested whether extensively trained avoidance impairs the subsequent goal-directed approach of rewards. Healthy participants were extensively trained to avoid an aversive outcome by performing simple responses to distinct full-screen color stimuli. After the subsequent devaluation of the aversive outcome, participants received monetary rewards for correct responses to neutral object pictures, which were presented on top of the same full-screen colors. These approach responses were either compatible or incompatible with habitual avoidance responses. Notably, the full-screen colors were not relevant to inform approach responses. In Experiment 1, participants were not instructed about post-devaluation stimulus-response-reward contingencies. Accuracy was lower in habit-incompatible than in habit-compatible trials, indicating costly avoidance, whereas reaction times did not differ. In Experiment 2, contingencies were explicitly instructed. Accuracy differences disappeared, but reaction times were slower in habit-incompatible than in habit-compatible trials, indicating low-cost habitual avoidance tendencies. These findings suggest a small but consistent impact of habitual avoidance tendencies on subsequent goal-directed approach. Costly habitual responding could, however, be inhibited when competing goal-directed approach was easily realizable.


Author(s):  
Bart Hartogsveld ◽  
Peter van Ruitenbeek ◽  
Conny W. E. M. Quaedflieg ◽  
Tom Smeets

Abstract. Instrumental learning is regulated by two memory systems: a relatively rigid but efficient habit system and a flexible but resource-demanding goal-directed system. Previous work has demonstrated that exposure to acute stress may shift the balance between these systems toward the habitual system. In the current study, we used a 2-day outcome devaluation paradigm with a 75% reward contingency rate and altered food reward categories to replicate and extend our previous findings. Participants learned neutral stimulus–response–reward associations on the first day. On the second day, rewards were devalued by eating to satiety. Subsequently, acute stress was induced in half of the participants using the Maastricht Acute Stress Test, while the other half engaged in a nonstressful control task. Finally, relative goal-directed versus habitual behavior was evaluated in a slips-of-action phase, where more slips-of-action indicate a shift toward the habitual system. Results showed that participants successfully acquired the stimulus–response–reward associations, that devaluation was effective, and that stressed participants displayed significant increases in cortisol and blood pressure. Stress led participants to commit more slips-of-action compared with nonstressed controls. The current study extends previous work, showing that the employed paradigm and outcome devaluation procedure are boundary conditions to the stress-induced shift in instrumental responding.


2021 ◽  
Author(s):  
Jacqueline Katharina Meier ◽  
Bernhard P. Staresina ◽  
Lars Schwabe

AbstractStress may shift behavioural control from a goal-directed system that encodes action-outcome relationships to a habit system that learns stimulus-response associations. Although this shift to habits is highly relevant for stress-related psychopathologies, limitations of existing behavioural paradigms hindered previous research to answer the fundamental question of whether the stress-induced bias to habits is due to impaired goal-directed or enhanced habitual processing (or both). Here, we leveraged EEG-based multivariate pattern analysis to decode neural outcome representations, crucial for goal-directed control, and response representations, essential for habitual responding, during instrumental learning. We show that stress reduces outcome representations but enhances response representations, both of which were directly associated with a behavioural index of habitual responding. Further, changes in outcome and response representations were uncorrelated, suggesting that these may reflect distinct processes. Our findings indicate that habit behaviour under stress is the result of both enhanced habitual and diminished goal-directed processing.


PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e8490
Author(s):  
María Sol Fanjul ◽  
Roxana R. Zenuto

Background Animal personalities have been studied in a wide variety of taxa, but among rodents, available studies are relatively scarce and have focused mainly on social species. In this study, we evaluated the existence of personality in the solitary subterranean rodent Ctenomys talarum. Specifically, we aimed to test individual differences in behavior that are stable over time and context in males of C. talarum captured in the wild. Methods Our experimental design included two series of three behavioral tests each, carried out with a 35 day time interval. Each series included an Open Field test, a Social Encounter test, and an Open Field test with a predator stimulus. Results Of the total recorded behaviors, 55.55% showed temporal consistency. Principal component analysis of consistent behaviors grouped them into four dimensions that explain inter individual behavioral variability, in order of importance: activity, socioaversion, boldness and exploration. Therefore, our results suggest that the concept of animal personality is applicable to C. talarum and the dimensions found are in accordance with the ecological and behavioral characteristics of this species.


Author(s):  
Heather C. Bell

From a stimulus-response (S-R) point of view, or even with an intermediate step, involving cognition (S-O-R), the existence of behavioral variablity in organisms, even under tightly controlled experimental conditions, suggests that 1) the relevant inputs to the system have not been fully characterized, 2) even the most minute difference in system inputs can produce vastly variable behavioral output, or 3) that behavior is fundamentally variable. Any of these possibilities leads to the conclusion that precise behavioral prediction, at any given moment, is virtually impossible. One can, however, re-conceptualize the challenge of understanding behavior such that it involves not what the organism will do from moment to moment, but what the characteristics of the system that governs the behavior of the organism are. In this paper, I outline a closed-loop cybernetic approach to understanding behavior, for which behavioral variability is actually a requirement. Findings are presented from a series of experiments across species, and using computer simulations, that support a cybernetic interpretation of behavior. I argue that behavioral variability provides adaptive advantages to organisms – regardless of whether that variability is produced by noise, or is actively generated by nervous systems. Finally, I discuss some ideas from embodied cognition that impose constraints on the variability of behavior.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Aref Arzan Zarin ◽  
Brandon Mark ◽  
Albert Cardona ◽  
Ashok Litwin-Kumar ◽  
Chris Q Doe

Animals generate diverse motor behaviors, yet how the same motor neurons (MNs) generate two distinct or antagonistic behaviors remains an open question. Here, we characterize Drosophila larval muscle activity patterns and premotor/motor circuits to understand how they generate forward and backward locomotion. We show that all body wall MNs are activated during both behaviors, but a subset of MNs change recruitment timing for each behavior. We used TEM to reconstruct a full segment of all 60 MNs and 236 premotor neurons (PMNs), including differentially-recruited MNs. Analysis of this comprehensive connectome identified PMN-MN ‘labeled line’ connectivity; PMN-MN combinatorial connectivity; asymmetric neuronal morphology; and PMN-MN circuit motifs that could all contribute to generating distinct behaviors. We generated a recurrent network model that reproduced the observed behaviors, and used functional optogenetics to validate selected model predictions. This PMN-MN connectome will provide a foundation for analyzing the full suite of larval behaviors.


Brain ◽  
2015 ◽  
Vol 139 (2) ◽  
pp. 605-615 ◽  
Author(s):  
Cécile Delorme ◽  
Alexandre Salvador ◽  
Romain Valabrègue ◽  
Emmanuel Roze ◽  
Stefano Palminteri ◽  
...  

Abstract Tics are sometimes described as voluntary movements performed in an automatic or habitual way. Here, we addressed the question of balance between goal-directed and habitual behavioural control in Gilles de la Tourette syndrome and formally tested the hypothesis of enhanced habit formation in these patients. To this aim, we administered a three-stage instrumental learning paradigm to 17 unmedicated and 17 antipsychotic-medicated patients with Gilles de la Tourette syndrome and matched controls. In the first stage of the task, participants learned stimulus-response-outcome associations. The subsequent outcome devaluation and ‘slip-of-action’ tests allowed evaluation of the participants’ capacity to flexibly adjust their behaviour to changes in action outcome value. In this task, unmedicated patients relied predominantly on habitual, outcome-insensitive behavioural control. Moreover, in these patients, the engagement in habitual responses correlated with more severe tics. Medicated patients performed at an intermediate level between unmedicated patients and controls. Using diffusion tensor imaging on a subset of patients, we also addressed whether the engagement in habitual responding was related to structural connectivity within cortico-striatal networks. We showed that engagement in habitual behaviour in patients with Gilles de la Tourette syndrome correlated with greater structural connectivity within the right motor cortico-striatal network. In unmedicated patients, stronger structural connectivity of the supplementary motor cortex with the sensorimotor putamen predicted more severe tics. Overall, our results indicate enhanced habit formation in unmedicated patients with Gilles de la Tourette syndrome. Aberrant reinforcement signals to the sensorimotor striatum may be fundamental for the formation of stimulus-response associations and may contribute to the habitual behaviour and tics of this syndrome.


2016 ◽  
Vol 7 (1) ◽  
Author(s):  
Dong Hoon Shin ◽  
Gyu-Hee Kim ◽  
Jin Soo Lee ◽  
In Soo Joo ◽  
Haeyoung Suh-Kim ◽  
...  

AbstractIntracerebral (IC) grafting of mesenchymal stem cells (MSCs) is not currently used in humans due to its potential complications. On the other hand, intra-arterial (IA) administration can be facilitated for engrafting of intensifed MSCs in the injured human brain. The study is designed to compare the two methods of MSC administration using IA and IC routes through the parameters of behavior, infarct volume, cell distribution, and MSC identification. An ischemic stroke model was generated in Sprague Dawley male rats. This experiment used MSCs/Ngn1 that express Neurogenin1 (Ngn1) to ensure grafted MSC maintenance. MSCs/Ngn1 or normal saline was administrated via the IC or IA route on day 3. All animals were randomly assigned into four groups (five rats in each group): IC-control, IA-control, IC-MSCs/Ngn1, or IA-MSCs/Ngn1. Motor behaviors, infarct volume, and distribution of superparamagnetic iron oxide (SPIO)-labeled cells on magnetic resonance imaging (MRI) were compared from each group. There were no baseline differencess in motor behaviors or infarct volume between IC-MSCs/Ngn1 and IA-MSCs/Ngn1. Hovever, the IA-MSCs/Ngn1 group showed the greatest recovery on Rotarod testing and adhesive removal tests (p = 0.003 and p = 0.009 vs. IC-MSCs/Ngn1, respectively). The IA-MSCs/Ngn1 group also had more evenly distributed SPIO-labeled cells on MRI. The results suggest that IA administration is likely to be benefcial for humans based on its ability to improve behavioral outcomes and ensure even MSC engrafting.


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