Information theory, novelty and hippocampal responses: unpredicted or unpredictable?

Shannon's information theory provides a principled framework for the quantitative analysis of brain responses during the encoding and representation of event streams. In particular, entropy measures the expected uncertainty of events in a given context. This contextual uncertainty or unpredictability may, itself, be important for balancing [bottom-up] sensory information and [top-down] prior expectations during perceptual synthesis. Using event-related functional magnetic resonance imaging (fMRI), we found that the anterior hippocampus is sensitive to the entropy of a visual stimulus stream. In contrast, activity in an extensive bilateral cortico-thalamic network was dictated by the surprise or information associated with each particular stimulus. In short, we show that the probabilistic structure or context in which events occur is an important predictor of hippocampal activity.

[1]  R. Dolan,et al.  Dissociating prefrontal and hippocampal function in episodic memory encoding , 1997, Nature.

[2]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[3]  Karl J. Friston.  Functional integration and inference in the brain , 2002, Progress in Neurobiology.

[4]  Geoffrey E. Hinton,et al.  The "wake-sleep" algorithm for unsupervised neural networks. , 1995, Science.

[5]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[6]  D. Mumford.  On the computational architecture of the neocortex , 2004, Biological Cybernetics.

[7]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[8]  Mitsuo Kawato,et al.  A forward-inverse optics model of reciprocal connections between visual cortical areas , 1993 .

[9]  Karen A. Daniels,et al.  Conscious and Unconscious Processing of Nonverbal Predictability in Wernicke's Area , 2000, The Journal of Neuroscience.

[10]  B. Strange,et al.  Adaptive anterior hippocampal responses to oddball stimuli , 2001, Hippocampus.

[11]  Geraint Rees,et al.  What can functional imaging reveal about the role of attention in visual awareness? , 2001, Neuropsychologia.

[12]  J. Rohrbaugh,et al.  Endogenous potentials generated in the human hippocampal formation and amygdala by infrequent events. , 1980, Science.

[13]  D. Schacter,et al.  Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval , 1999, Hippocampus.

[14]  E. Tulving,et al.  Hippocampal PET activations of memory encoding and retrieval: The HIPER model , 1998, Hippocampus.

[15]  D. S. Jones,et al.  Elementary information theory , 1979 .

[16]  C. I. Hovland,et al.  Transmission of information concerning concepts through positive and negative instances. , 1953, Journal of experimental psychology.

[17]  M. Hasselmo,et al.  Encoding and retrieval of episodic memories: Role of cholinergic and GABAergic modulation in the hippocampus , 1998, Hippocampus.

[18]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[19]  H. Eichenbaum,et al.  The Hippocampus, Memory, and Place Cells Is It Spatial Memory or a Memory Space? , 1999, Neuron.

[20]  R. Hyman.  Stimulus information as a determinant of reaction time. , 1953, Journal of experimental psychology.

[21]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[22]  P. Matthews,et al.  Learning about pain: the neural substrate of the prediction error for aversive events. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[24]  Janne Sinkkonen.  Information and Resource Allocation , 2000, Information Theory and the Brain.

[25]  Karl J. Friston,et al.  Segregating the functions of human hippocampus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  P. Ashworth,et al.  Handbook of Implicit Learning , 1998 .

[27]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[28]  F. Craik,et al.  Novelty and familiarity activations in PET studies of memory encoding and retrieval. , 1996, Cerebral cortex.

[29]  D Mumford,et al.  On the computational architecture of the neocortex. II. The role of cortico-cortical loops. , 1992, Biological cybernetics.

[30]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[31]  Peter Dayan,et al.  Acetylcholine in cortical inference , 2002, Neural Networks.

[32]  Peter J. B. Hancock,et al.  Information Theory and the Brain , 2000 .

[33]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[34]  W. E. Hick.  Quarterly Journal of Experimental Psychology , 1948, Nature.

[35]  M. W. Brown,et al.  Recognition memory: neuronal substrates of the judgement of prior occurrence , 1998, Progress in Neurobiology.

[36]  P. Goldman-Rakic,et al.  Infrequent events transiently activate human prefrontal and parietal cortex as measured by functional MRI. , 1997, Journal of neurophysiology.

[37]  Leslie G. Ungerleider,et al.  What fMRI has taught us about human vision , 1997, Current Opinion in Neurobiology.