Brain, Vol. 126, No. 7, 1509-1510,
July 2003
© 2003 Guarantors of Brain
doi: 10.1093/brain/awg212
Editorial |
In search of one’s own past: the neural bases of autobiographical memories
1 Institute of Medicine, Research Centre Jülich and Department of Neurology, RWTH Aachen, Aachen, Germany
It is more than a century ago that Francis Galton (1879
) introduced in this very journal what is now often considered to be the first empirical study of autobiographical memory: ‘I propose in this memoir to give a new instance of psychometry, and a few of its results. ... I trust ... the readers ... will be prepared to agree with the view, that until the phenomena of any branch of knowledge have been subjected to measurement and number, it cannot assume the status and dignity of a science.’
Early efforts to understand where memories are stored in the brain were relatively unsuccessful until Penfield and Perot (1963), using direct electrical stimulation of the exposed neocortex of epilepsy patients, discovered that stimulation of a particular region in the temporal neocortex elicited what seemed to be autobiographical memories. Their neurophysiologically based claim that autobiographical memories rely on temporal neocortex was weakened, however, by the finding that the same areas could be surgically removed without the memories being lost. In contrast, several case studies (including, for example, the now famous case of H.M. who underwent bilateral MTL surgery for relief of epilepsy) linked defects in episodic memory to damage to the medial temporal lobes (MTL) (Scoville and Milner, 1957), and in particular the hippocampal formation together with perirhinal and entorhinal cortex. Interestingly, patients with MTL damage lose recent rather than remote memories. This observation suggests that episodic memories gradually become independent of the MTL—a finding that fitted Ribot’s law (Ribot, 1882) quite well: ‘The progressive destruction of memory follows a logical order—a law. ... it begins with the most recent recollections which, being ... rarely repeated and ... having no permanent associations represent organisation in its feeblest form.’ If episodic memories become independent of the MTL with time, then surely they must be transferred and stored somewhere else? Based upon largely animal data (Hoffman and McNaughton, 2002) the currently prevailing view is that each episodic event leaves a trace in our brain which initially is created in neocortex, then gets stored in MTL but thereafter gradually becomes independent of MTL and established in distributed neocortical networks by consolidation (i.e. the processes operating during the time after learning that allow information to be retained in memory). It is, at least in part, this complex and distributed nature of the neural processes underpinning autobiographical memory that has made studying it so difficult.
Even today human neurophysiological data of how neurons form autobiographical memories are scarce: the wealth of electrophysiological and functional neuroimaging studies on the encoding and retrieval of semantic and episodic (non-autobiographical) memory employing highly elaborated paradigms from cognitive neuropsychology (often showing prefrontal activations but failing to show hippocampal involvement) contrasts with the dearth of data on the neural mechanisms associated with autobiographical memory. Although autobiographical memory has become a topic of immense research interest over the last 30 years, the cerebral representation of one’s own past remains to be elucidated. Despite the fact that long-term autobiographical memory constitutes a key component of self-consciousness (consciousness of ‘self’), the search for the underlying neurophysiological correlates to it has proven difficult for reasons beyond its distributed nature. For example, by necessity, autobiographical memory is normally linked to the awareness of the time course of one’s own life history and hence can be specifically engaged in the meaningful reconstruction of one’s own past (Fink et al., 1996). Furthermore, the recollective experience is often related to the evocation of previously experienced emotions. Due to this highly complex interaction of cognitive and emotional processes, the experimental investigation of the neural bases of autobiographical memory remains a challenge to basic and clinical neuro scientists (Fink et al., 1996).
Despite these issues, functional neuroimaging is a powerful tool which allows new insights into the neural correlates of emotion-laden autobiographical memory. Recently, functional neuroimaging has demonstrated differentially increased neural activity bilaterally in the hippocampal region associated with the recall of recent but not remote autobiographical memories (Piefke et al., 2003). The results of Piefke and co-workers confirm that the brain regions involved in autobiographical memory retrieval are influenced by the triggered memories’ relationship to the individual time axis and that memory consolidation might indeed be based on medial temporal–neocortical interactions, as suggested by neuropsychological studies of patients with MTL damage. Interestingly, the observation of such a time-dependent involvement of the hippocampal region in memory consolidation also parallels the course of retrograde amnesia observed in dementing patients suffering from Alzheimer’s disease, with the loss of recent memories appearing during early stages of the disease when conspicuous neurofibrillary changes are restricted mainly to the hippocampal and parahippocampal regions. Only during later stages, as the neurofibrillary changes spread out to neocortical association areas, do remote memories also become impaired.
In this issue of Brain, Maguire and Frith (2003) now take one of the core issues of autobiographical memory further by providing the first data on the effects of normal ageing on the neural correlates of remembering real life events. Maguire and Frith studied young and elderly subjects using fMRI while they retrieved real life autobiographical events. Taking great care to ensure that the stimuli, tasks and performance level of both groups were comparable they show that the left and right hippocampal regions are differentially involved in autobiographical memory retrieval with increasing age: while only left hippocampal activation was evident in the young, bilateral hippocampal activation became apparent in the older adults. This differential hippocampal involvement with increasing age was not observed for semantic memories nor was it related to morphological changes in the MTL regions associated with ageing. Maguire and Frith thus highlight the necessity of refining our knowledge of the hippocampal role in autobiographical memory: understanding the pathophysiology of memory disorders associated with diseases that affect the MTL (e.g. Alzheimer’s disease) necessitates an understanding of the physiological dynamic plasticity of the functional anatomy of memory networks.
A frequent criticism of functional neuroimaging is that it offers limited additional information to that obtained from lesion studies. Studies of autobiographical memory prove this criticism wrong: functional neuroimaging has allowed and continues to allow us new insights into both the neural networks and processes underlying autobiographical memories. Exciting new approaches to the study of autobiographical memory including the assessment of altered patterns of effective connectivity between affected and unaffected brain regions (Maguire et al., 2001) and the neurochemical bases of memories (Thiel et al., 2002) are at hand. It is only the combined evidence of functional imaging and neuropsychological studies that will further our knowledge of both neurological and psychiatric (Markowitsch et al., 1997) disorders of autobiographical memories.
References
Fink GR, Markowitsch HJ, Reinkemeier M, Bruckbauer T, Kessler J, Heiss W-D. Cerebral representation of one’s own past: neural networks involved in autobiographical memory. J Neurosci 1996; 16: 4275–82.
Galton F. Psychometric experiments. Brain 1879; 2: 149–62.
Hoffman KL, McNaughton BL. Coordinated reactivation of distributed memory traces in primate neocortex. Science 2002; 297: 2070–73.
Maguire EA, Frith CD. Aging affects the engagement of the hippocampus during autobiographical memory retrieval. Brain 2003; 126: 1511–1523.
Maguire EA, Vargha-Khadem F, Mishkin M. The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 2001; 124: 1156–70.
Markowitsch HJ, Fink GR, Thöne AIM, Kessler J, Heiss W-D. Persistent psychogenic amnesia with a PET-proven organic basis. Cogn Neuropsychiatry 1997; 2: 135–58.[CrossRef]
Penfield W, Perot P. The brain’s record of auditory and visual experience. Brain 1963; 86: 595–696.
Piefke M, Weiss PH, Zilles K, Markowitsch HJ, Fink GR. Differential remoteness and emotional tone modulate the neural correlates of autobiographical memories. Brain 2003; 126: 650–68.
Ribot T. Diseases of memory. New York: Appleton; 1882.
Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 1957; 20: 11–21.[ISI][Medline]
Thiel CM, Friston KJ, Dolan RJ. Cholinergic modulation of experience-dependent plasticity in human auditory cortex. Neuron 2002; 35: 567–74.[CrossRef][ISI][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  S. J. Gilbert, S. Spengler, J. S. Simons, J. D. Steele, S. M. Lawrie, C. D. Frith, and P. W. Burgess Functional Specialization within Rostral Prefrontal Cortex (Area 10): A Meta-analysis. J. Cogn. Neurosci., June 1, 2006; 18(6): 932 - 948. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||