Contribution of dorsal versus ventral hippocampus to the hierarchical modulation of goal-directed action

Adaptive behavior often necessitates that animals learn about events in a manner that is specific to a particular context or environment. These hierarchical organizations allow the animal to decide which action is the most appropriate when faced with ambiguous or conflicting possibilities. This study examined the role of hippocampus in enabling animals to use the context to guide action selection. We used a hierarchical instrumental outcome devaluation task in which male rats learn that the context provides information about the unique action-outcome relations that are in effect. We first confirmed that rats encode and use hierarchical context-(action-outcome) relations. We then show that chemogenetic inhibition of ventral hippocampus (vHPC) impairs both the encoding and retrieval of these associations, while inhibition of dorsal hippocampus (dHPC) impairs only the retrieval. Importantly, neither dHPC or vHPC were required for goal-directed behavior per se as these impairments only emerged when rats were forced to use the context to identify the current action-outcome relationships. These findings are discussed with respect to the role of the hippocampus and its broader circuitry in the contextual modulation of goal-directed behavior and the importance of hierarchical associations in flexible behavior.

[1]  Jeremy S. Biane,et al.  Neural dynamics underlying associative learning in the dorsal and ventral hippocampus , 2023, Nature Neuroscience.

[2]  R. Monasson,et al.  A synaptic signal for novelty processing in the hippocampus , 2022, Nature Communications.

[3]  B. Balleine,et al.  Response-independent outcome presentations weaken the instrumental response-outcome association. , 2021, Journal of experimental psychology. Animal learning and cognition.

[4]  M. Bouton Context, attention, and the switch between habit and goal-direction in behavior , 2021, Learning & Behavior.

[5]  L. Chandler,et al.  Behavioral and slice electrophysiological assessment of DREADD ligand, deschloroclozapine (DCZ) in rats , 2021, Scientific Reports.

[6]  Kenji F. Tanaka,et al.  Chronic social defeat stress impairs goal-directed behavior through dysregulation of ventral hippocampal activity in male mice , 2021, Neuropsychopharmacology.

[7]  Stephen Maren,et al.  Ventral hippocampus mediates the context-dependence of two-way signaled avoidance in male rats , 2021, Neurobiology of Learning and Memory.

[8]  J. Gordon,et al.  Reset of hippocampal-prefrontal circuitry facilitates learning , 2021, Nature.

[9]  Kathleen G Bryant,et al.  Arbitration of Approach-Avoidance Conflict by Ventral Hippocampus , 2020, Frontiers in Neuroscience.

[10]  M. Joesch,et al.  Ventro-dorsal Hippocampal Pathway Gates Novelty-Induced Contextual Memory Formation , 2020, Current Biology.

[11]  M. Stanton,et al.  Role of dorsal and ventral hippocampal muscarinic receptor activity in acquisition and retention of contextual fear conditioning. , 2020, Behavioral neuroscience.

[12]  Laura A. Bradfield,et al.  Goal-directed actions transiently depend on dorsal hippocampus , 2020, Nature Neuroscience.

[13]  J. Kim,et al.  Dissociated roles of dorsal and ventral hippocampus in recall and extinction of conditioned fear in male and female juvenile rats , 2020, Experimental Neurology.

[14]  Samuel T. Slocum,et al.  Deschloroclozapine, a potent and selective chemogenetic actuator enables rapid neuronal and behavioral modulations in mice and monkeys , 2019, Nature Neuroscience.

[15]  S. Gourley,et al.  Glucocorticoid-sensitive ventral hippocampal-orbitofrontal cortical connections support goal-directed action – Curt Richter Award Paper 2019 , 2019, Psychoneuroendocrinology.

[16]  Kenji F. Tanaka,et al.  Serotonin-mediated inhibition of ventral hippocampus is required for sustained goal-directed behavior , 2019, Nature Neuroscience.

[17]  Bernard W. Balleine,et al.  The Bilateral Prefronto-striatal Pathway Is Necessary for Learning New Goal-Directed Actions , 2018, Current Biology.

[18]  Adam G. Carter,et al.  Ventral Hippocampal Inputs Preferentially Drive Corticocortical Neurons in the Infralimbic Prefrontal Cortex , 2018, The Journal of Neuroscience.

[19]  Laura A. Bradfield,et al.  Prefrontal Corticostriatal Disconnection Blocks the Acquisition of Goal-Directed Action , 2018, The Journal of Neuroscience.

[20]  K. Ressler,et al.  Regulation of actions and habits by ventral hippocampal trkB and adolescent corticosteroid exposure , 2017, PLoS biology.

[21]  Matthijs A. A. van der Meer,et al.  Ventral, but not dorsal, hippocampus inactivation impairs reward memory expression and retrieval in contexts defined by proximal cues , 2017, Hippocampus.

[22]  M. Bouton,et al.  Occasion setting, inhibition, and the contextual control of extinction in Pavlovian and instrumental (operant) learning , 2017, Behavioural Processes.

[23]  B. Balleine,et al.  Consolidation of Goal-Directed Action Depends on MAPK/ERK Signaling in Rodent Prelimbic Cortex , 2016, The Journal of Neuroscience.

[24]  Iryna Filippava,et al.  Goal Directed Action , 2015 .

[25]  S. Killcross,et al.  The prelimbic cortex uses contextual cues to modulate responding towards predictive stimuli during fear renewal , 2015, Neurobiology of Learning and Memory.

[26]  Alexandra T. Keinath,et al.  Precise spatial coding is preserved along the longitudinal hippocampal axis , 2014, Hippocampus.

[27]  M. Bouton,et al.  Contextual control of operant behavior: evidence for hierarchical associations in instrumental learning , 2014, Learning & behavior.

[28]  Mark E. Bouton,et al.  A fundamental role for context in instrumental learning and extinction , 2014, Behavioural Processes.

[29]  G. Urcelay,et al.  The functions of contexts in associative learning , 2014, Behavioural Processes.

[30]  S. Killcross,et al.  The prelimbic cortex contributes to the down-regulation of attention toward redundant cues. , 2014, Cerebral cortex.

[31]  H. Scharfman,et al.  Expression of c‐fos in hilar mossy cells of the dentate gyrus in vivo , 2013, Hippocampus.

[32]  I. Muzzio,et al.  Differential roles of the dorsal and ventral hippocampus in predator odor contextual fear conditioning , 2013, Hippocampus.

[33]  Inah Lee,et al.  Contextual behavior and neural circuits , 2013, Front. Neural Circuits.

[34]  K. Luan Phan,et al.  The contextual brain: implications for fear conditioning, extinction and psychopathology , 2013, Nature Reviews Neuroscience.

[35]  Howard Eichenbaum,et al.  Ventral Hippocampal Neurons Are Shaped by Experience to Represent Behaviorally Relevant Contexts , 2013, The Journal of Neuroscience.

[36]  Travis P. Todd Mechanisms of renewal after the extinction of instrumental behavior. , 2013, Journal of experimental psychology. Animal behavior processes.

[37]  B. Roth,et al.  Remote Control of Neuronal Signaling , 2011, Pharmacological Reviews.

[38]  M. Bouton,et al.  Renewal after the extinction of free operant behavior , 2011, Learning & behavior.

[39]  Shoji Nakamura,et al.  Electrophysiological analysis of the loop neural circuit between the medial prefrontal cortex and amygdala in the rat , 2010, Neuroscience Research.

[40]  JaneR . Taylor,et al.  Dissociable regulation of instrumental action within mouse prefrontal cortex , 2010, The European journal of neuroscience.

[41]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[42]  Jerry W Rudy,et al.  Context representations, context functions, and the parahippocampal-hippocampal system. , 2009, Learning & memory.

[43]  S. Killcross,et al.  Contextual control of biconditional task performance: Evidence for cue and response competition in rats , 2008, Quarterly journal of experimental psychology.

[44]  S. Floresco,et al.  Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure , 2008, Behavioural Brain Research.

[45]  Guy Sandner,et al.  Rewarded associative and instrumental conditioning after neonatal ventral hippocampus lesions in rats , 2008, Brain Research.

[46]  S. Killcross,et al.  Contextual Control of Choice Performance , 2007, Annals of the New York Academy of Sciences.

[47]  B. Roth,et al.  Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand , 2007, Proceedings of the National Academy of Sciences.

[48]  S. Killcross,et al.  Inactivation of the prelimbic, but not infralimbic, prefrontal cortex impairs the contextual control of response conflict in rats , 2007, The European journal of neuroscience.

[49]  Shoji Nakamura,et al.  Ventral hippocampal neurons project axons simultaneously to the medial prefrontal cortex and amygdala in the rat. , 2006, Journal of neurophysiology.

[50]  S. Killcross,et al.  Prefrontal Cortex Lesions Disrupt the Contextual Control of Response Conflict , 2006, The Journal of Neuroscience.

[51]  Jennifer A. Hobin,et al.  Ventral hippocampal muscimol disrupts context‐specific fear memory retrieval after extinction in rats , 2006, Hippocampus.

[52]  B. Balleine,et al.  The role of prelimbic cortex in instrumental conditioning , 2003, Behavioural Brain Research.

[53]  S. Killcross,et al.  Coordination of actions and habits in the medial prefrontal cortex of rats. , 2003, Cerebral cortex.

[54]  B. Balleine,et al.  Sensitivity to Instrumental Contingency Degradation Is Mediated by the Entorhinal Cortex and Its Efferents via the Dorsal Hippocampus , 2002, The Journal of Neuroscience.

[55]  V. Brown,et al.  Medial Frontal Cortex Mediates Perceptual Attentional Set Shifting in the Rat , 2000, The Journal of Neuroscience.

[56]  Stephen Maren,et al.  Muscimol Inactivation of the Dorsal Hippocampus Impairs Contextual Retrieval of Fear Memory , 1999, The Journal of Neuroscience.

[57]  B. Balleine,et al.  Goal-directed instrumental action: contingency and incentive learning and their cortical substrates , 1998, Neuropharmacology.

[58]  B. Balleine,et al.  Bidirectional Instrumental Conditioning , 1996, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[59]  M. Gluck,et al.  Context, conditioning, and hippocampal rerepresentation in animal learning. , 1994, Behavioral neuroscience.

[60]  M. Bouton Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. , 1993, Psychological bulletin.

[61]  R. Rescorla Hierarchical Associative Relations in Pavlovian Conditioning and Instrumental Training , 1992 .

[62]  T. Jay,et al.  Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris‐leucoagglutinin , 1991, The Journal of comparative neurology.

[63]  R. Rescorla,et al.  Evidence for the hierarchical structure of instrumental learning , 1990 .

[64]  M. Bouton,et al.  Analysis of the associative and occasion-setting properties of contexts participating in a Pavlovian discrimination. , 1986 .

[65]  Laura A. Bradfield,et al.  The contextual regulation of goal-directed actions , 2021, Current Opinion in Behavioral Sciences.

[66]  吉田 慶多朗 Serotonin-mediated inhibition of ventral hippocampus is required for sustained goal-directed behavior (要旨) , 2019 .

[67]  M. Bouton,et al.  Contextual control of instrumental actions and habits. , 2015, Journal of experimental psychology. Animal learning and cognition.

[68]  Samuel P. León,et al.  Contextual control of discriminated operant behavior. , 2014, Journal of Experimental Psychology: Animal Learning and Cognition.

[69]  Laura A. Bradfield,et al.  Hierarchical and binary associations compete for behavioral control during instrumental biconditional discrimination. , 2013, Journal of experimental psychology. Animal behavior processes.

[70]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[71]  R. J. Meijer,et al.  Collateral projections from the rat hippocampal formation to the lateral and medial prefrontal cortex , 1997, Hippocampus.

[72]  J. Cohen,et al.  Context, cortex, and dopamine: a connectionist approach to behavior and biology in schizophrenia. , 1992, Psychological review.