Preserved complex emotion-based learning in amnesia

https://doi.org/10.1016/j.neuropsychologia.2005.04.019Get rights and content

Abstract

An important role for emotion in decision-making has recently been highlighted by disruptions in problem solving abilities after lesion to the frontal lobes. Such complex decision-making skills appear to be based on a class of memory ability (emotion-based learning) that may be anatomically independent of hippocampally mediated episodic memory systems. There have long been reports of intact emotion-based learning in amnesia, arguably dating back to the classic report of Claparede. However, all such accounts relate to relatively simple patterns of emotional valence learning, rather than the more complex contingency patterns of emotional experience, which characterise everyday life. A patient, SL, who had a profound anterograde amnesia following posterior cerebral artery infarction, performed a measure of complex emotion-based learning (the Iowa Gambling Task) on three separate occasions. Despite his severe episodic memory impairment, he showed normal levels of performance on the Gambling Task, at levels comparable or better than controls—including learning that persisted across substantial periods of time (weeks). Thus, emotion-based learning systems appear able to encode, and sustain, more sophisticated patterns of valence learning than have previously been reported.

Section snippets

History

SL was an 85-year-old married man, with two grown up children, who worked as a building inspector before he retired. He suffered a posterior cerebral artery stroke in late 2003, 2 months prior to the initial assessment. CT scans indicated a large hypodense area across almost all of the left posterior cerebral artery territory, consistent with a recent infarct (see Fig. 1). On the left side, the lesion involved the medial and lateral surfaces of the occipital lobe, as well as the infero-medial

Results

Data were analysed in two separate ways: firstly, to observe whether there was learning during the individual sessions, and secondly whether there were any cumulative effects of learning across sessions.

Discussion

The key aim of the present study was to evaluate the performance of an amnesic patient on a measure of complex emotion-based learning. SL presented with a profound impairment of recent episodic memory, as shown by a range of floor, or chance, performances. In contrast, he showed reasonable levels of performance on tasks of immediate/working memory. This pattern of performance is entirely consistent with the sorts of episodic amnesia typically observed after lesion to the hippocampal memory

Acknowledgement

We would like to thank Prof. Robert Rafal for his assistance with the neurological and neuroradiological aspects of the paper.

This research was funded by the National Alliance for Research on Schizophrenia and Depression (NARSAD) and the Wellcome Trust.

References (53)

  • T. Shallice et al.

    The involvement of the frontal lobes in cognitive estimation

    Cortex

    (1978)
  • O.H. Turnbull et al.

    Direct versus indirect emotional consequences on the Iowa Gambling Task

    Brain and Cognition

    (2003)
  • D.J. Barraclough et al.

    Prefrontal cortex and decision-making in a mixed-strategy game

    Nature Neuroscience

    (2004)
  • A. Bechara

    A neural view of the regulation of complex cognitive functions by emotion

  • A. Bechara et al.

    Emotion, decision-making and the orbitofrontal cortex

    Cerebral Cortex

    (2000)
  • A. Bechara et al.

    Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making

    The Journal of Neuroscience

    (1999)
  • A. Bechara et al.

    Deciding advantageously before knowing the advantageous strategy

    Science

    (1997)
  • A. Bechara et al.

    Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex

    Cerebral Cortex

    (1996)
  • A.L. Benton et al.

    Multilingual aphasia examination

    (1989)
  • W.K. Bickel et al.

    The behavioural economics of concurrent drug reinforcers—A review and reanalysis of drug self-administration research

    Psychopharmacology

    (1995)
  • A.J. Cadler et al.

    Neuropsychology of fear and loathing

    Nature Reviews

    (2001)
  • E. Claparede

    Recognition and “me”ness

  • A.R. Damasio

    Descartes’ error: Emotion, reason, and the human brain

    (1994)
  • A.R. Damasio
    (1996)
  • A.R. Damasio et al.

    Amnesia caused by herpes simplex encephalitis, infarctions in basal forebrain, Alzheimer's disease, and anoxia

  • H. Eichenbaum et al.

    From conditioning to conscious recollection: Memory systems of the brain

    (2001)
  • Cited by (43)

    • Frontal-subcortical circuitry in social attachment and relationships: A cross-sectional fMRI ALE meta-analysis

      2017, Behavioural Brain Research
      Citation Excerpt :

      Emotional decision making has been informed by research on autonomic nervous system changes in response to social stimuli [18–21] and lesion studies of the ventral-medial prefrontal, amygdala, insula, and cerebellar regions [19,20,22,23]. Although emotion-based learning is dissociable from the episodic memory system [6,15,24–26], clearly they are interrelated in forming a historical precedent for the adaptive or maladaptive behavior an individual might display. Teuber [27] first reported a clear dissociation between people “knowing” what they should do but, instead, “doing” something different.

    • The role of the hippocampus in approach-avoidance conflict decision-making: Evidence from rodent and human studies

      2016, Behavioural Brain Research
      Citation Excerpt :

      Since the early seminal work of Scoville and Milner [98] and O’Keefe and colleagues [9,99], neuropsychological research on the human HPC has focused traditionally on the detrimental effects of HPC lesions on declarative (in particular episodic) memory and spatial cognition [8,100,101]. Although more recent work has extended the boundaries of this work to other domains including imagination [102], future thinking [103], working memory [104], perception [105], and memory- and/or future thinking-driven decision-making [106–108] there have, to our knowledge, been no clear reports of impaired approach-avoidance conflict processing in HPC-damaged patients (see also related work on the effects of HPC damage on decision-making in the context of gambling tasks e.g. [109–111]). The patient findings of Bach et al. [95] offer, therefore, some convergence with the rodent HPC lesion conflict literature and suggest that changes in human approach-avoidance behaviour following HPC dysfunction can be detected in the context of a carefully designed approach-avoidance conflict task.

    • Decision making under stress: A selective review

      2012, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      Working memory is also prone to stress-induced changes that may influence feedback learning. While some authors consider working memory an important mediator for learning under uncertain conditions (Hinson et al., 2002; Jameson et al., 2004), others emphasize that learning through somatic markers may occur with low executive involvement (Turnbull et al., 2005) and without intact episodic memory (Turnbull and Evans, 2006). Reward and punishment sensitivity should play a role in all decisions that offer reward or punishment.

    • Decision making under ambiguity in temporal lobe epilepsy: Does the location of the underlying structural abnormality matter?

      2011, Epilepsy and Behavior
      Citation Excerpt :

      Mesial temporal lobe structures are essential to adequate emotional processing, learning from reward, and adapting decisions after feedback [11], as well as in declarative memory. The contribution of declarative memory to decision making under ambiguity has been discussed controversially in the literature [29–31]. In the present study, the two TLE groups were comparable in performance on the verbal memory task, but markedly different in decision making.

    View all citing articles on Scopus
    View full text