Object Recognition and Sensitive Periods: A Computational Analysis of Visual Imprinting

Using neural and behavioral constraints from a relatively simple biological visual system, we evaluate the mechanism and behavioral implications of a model of invariant object recognition. Evidence from a variety of methods suggests that a localized portion of the domestic chick brain, the intermediate and medial hyperstriatum ventrale (IMHV), is critical for object recognition. We have developed a neural network model of translation-invariant object recognition that incorporates features of the neural circuitry of IMHV, and exhibits behavior qualitatively similar to a range of findings in the filial imprinting paradigm. We derive several counter-intuitive behavioral predictions that depend critically upon the biologically derived features of the model. In particular, we propose that the recurrent excitatory and lateral inhibitory circuitry in the model, and observed in IMHV, produces hysteresis on the activation state of the units in the model and the principal excitatory neurons in IMHV. Hysteresis, when combined with a simple Hebbian covariance learning mechanism, has been shown in this and earlier work (Fldik 1991; O'Reilly and McClelland 1992) to produce translation-invariant visual representations. The hysteresis and learning rule are responsible for a sensitive period phenomenon in the network, and for a series of novel temporal blending phenomena. These effects are empirically testable. Further, physiological and anatomical features of mammalian visual cortex support a hysteresis-based mechanism, arguing for the generality of the algorithm.

[1]  K. Lorenz The Companion in the Bird's World , 1937 .

[2]  J. Jaynes Imprinting: the interaction of learned and innate behavior. I. Development and generalization. , 1956, Journal of comparative and physiological psychology.

[3]  J. Jaynes Imprinting: the interaction of learned and innate behavior. IV. Generalization and emergent discrimination. , 1958, Journal of comparative and physiological psychology.

[4]  W. Sluckin,et al.  Imprinting and Perceptual Learning , 1961 .

[5]  W. K. Honig,et al.  Stimulus Generalization of Imprinting , 1961, Science.

[6]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[7]  J. Hailman,et al.  Perceptual Preferences and Imprinting in Chicks , 1964, Science.

[8]  Peter Secretan,et al.  Imprinting and Early Learning , 1965, Mental Health.

[9]  P. Bateson THE CHARACTERISTICS AND CONTEXT OF IMPRINTING , 1966, Biological reviews of the Cambridge Philosophical Society.

[10]  P. Klopfer Stimulus Preferences and Imprinting , 1967, Science.

[11]  E. Salzen,et al.  Reversibility of imprinting. , 1968, Journal of comparative and physiological psychology.

[12]  H. Hoffman,et al.  A reinforcement model of imprinting: Implications for socialization in monkeys and men. , 1973 .

[13]  D. Chantrey Stimulus preexposure and discrimination learning by domestic chicks: effect of varying interstimulus time. , 1974, Journal of comparative and physiological psychology.

[14]  A. Einsiedel The development and modification of object preferences in domestic white leghorn chicks. , 1975, Developmental psychobiology.

[15]  D. Stewart,et al.  Learning in domestic chicks after exposure to both discriminanda. , 1977 .

[16]  T. Sejnowski,et al.  Storing covariance with nonlinearly interacting neurons , 1977, Journal of mathematical biology.

[17]  L. J. Shapiro,et al.  The Effect of Enforced Exposure to Live Models on The Reversibility of Attachments in White Peking Ducklings , 1978 .

[18]  James L. McClelland,et al.  An interactive activation model of context effects in letter perception: I. An account of basic findings. , 1981 .

[19]  G. Horn,et al.  Differential effects of exposure to an imprinting stimulus on ‘spontaneous’ neuronal activity in two regions of the chick brain , 1982, Brain Research.

[20]  Carry Kertzman,et al.  Irreversibility of imprinting after active versus passive exposure to the object. , 1982 .

[21]  J J Hopfield,et al.  Neurons with graded response have collective computational properties like those of two-state neurons. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[22]  S. Rose,et al.  Differential 2-deoxyglucose uptake into chick brain structures during passive avoidance training , 1984, Neuroscience.

[23]  G. Horn,et al.  Changes in the structure of synapses associated with learning , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  G. Horn Memory, imprinting, and the brain : an inquiry into mechanisms , 1985 .

[25]  G. Horn,et al.  Connections of the hyperstriatum ventrale of the domestic chick (Gallus domesticus). , 1985, Journal of anatomy.

[26]  Tomaso Poggio,et al.  Computational vision and regularization theory , 1985, Nature.

[27]  David Zipser,et al.  Feature Discovery by Competive Learning , 1986, Cogn. Sci..

[28]  M. Johnson,et al.  Dissociation of recognition memory and associative learning by a restricted lesion of the chick forebrain , 1986, Neuropsychologia.

[29]  J. Kent Experiments on the relationship between the hen and chick (Gallus gallus): the role of the auditory mode in recognition and the effects of maternal separation , 1987 .

[30]  J. Rauschecker,et al.  Imprinting and cortical plasticity , 1987 .

[31]  G. Horn,et al.  The role of a restricted region of the chick forebrain in the recognition of individual conspecifics , 1987, Behavioural Brain Research.

[32]  T. Bliss,et al.  NMDA receptors - their role in long-term potentiation , 1987, Trends in Neurosciences.

[33]  Y. Frégnac,et al.  A cellular analogue of visual cortical plasticity , 1988, Nature.

[34]  J. Rauschecker,et al.  Imprinting and cortical plasticity. Comparative aspects of sensitive periods Edited by J. P. Rauschecker and P. Nader. Wiley Series in Neuroscience. 1987, 377 pages, £57.50. , 1988, Neuropsychologia.

[35]  Y. Frégnac,et al.  A cellular analogue of visual cortical plasticity , 1988, Nature.

[36]  A. Csillag,et al.  Cell types of the hyperstriatum ventrale of the domestic chicken (Gallus domesticus): a Golgi study. , 1988, Journal fur Hirnforschung.

[37]  G. Horn,et al.  Learning and memory: regional changes in N-methyl-D-aspartate receptors in the chick brain after imprinting. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Dawn M. Taylor,et al.  The effects of hyperstriatal lesions on one-trial passive-avoidance learning in the chick , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  James L. McClelland,et al.  An interactive activation model of context effects in letter perception: part 1.: an account of basic findings , 1988 .

[40]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[41]  Kevan A. C. Martin,et al.  A Canonical Microcircuit for Neocortex , 1989, Neural Computation.

[42]  T. Sejnowski,et al.  Associative long-term depression in the hippocampus induced by hebbian covariance , 1989, Nature.

[43]  M. Johnson,et al.  Memory systems in the chick: Dissociations and neuronal analysis , 1989, Neuropsychologia.

[44]  Michael McCloskey,et al.  Catastrophic Interference in Connectionist Networks: The Sequential Learning Problem , 1989 .

[45]  Mark H. Johnson,et al.  Long-lasting effects of IMHV lesions on social preferences in domestic fowl. , 1989 .

[46]  T. Nealey,et al.  Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  G. Barrionuevo,et al.  Heterosynaptic correlates of long-term potentiation induction in hippocampal CA3 neurons , 1990, Neuroscience.

[48]  Alan L. Yuille,et al.  Generalized Deformable Models, Statistical Physics, and Matching Problems , 1990, Neural Computation.

[49]  P. Bateson,et al.  The importance of being first: a primacy effect in filial imprinting , 1990, Animal Behaviour.

[50]  W. Singer,et al.  Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex , 1990, Nature.

[51]  Mark H. Johnson Kin recognition: Information processing and storage during filial imprinting , 1991 .

[52]  Johan J. Bolhuis,et al.  MECHANISMS OF AVIAN IMPRINTING: A REVIEW , 1991, Biological reviews of the Cambridge Philosophical Society.

[53]  Peter Földiák,et al.  Learning Invariance from Transformation Sequences , 1991, Neural Comput..

[54]  D. Mitchell The long-term effectiveness of different regimens of occlusion on recovery from early monocular deprivation in kittens. , 1991, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[55]  S. Rose How chicks make memories: the cellular cascade from c-fos to dendritic remodelling , 1991, Trends in Neurosciences.

[56]  Tomaso Poggio,et al.  Computational vision and regularization theory , 1985, Nature.

[57]  G. Horn,et al.  The development of hemispheric asymmetries in neuronal activity in the domestic chick after visual experience , 1991, Behavioural Brain Research.

[58]  Mark H. Johnson,et al.  Biology and Cognitive Development: The Case of Face Recognition , 1993 .

[59]  Rodney J. Douglas,et al.  Synchronization of Bursting Action Potential Discharge in a Model Network of Neocortical Neurons , 1991, Neural Computation.

[60]  G. Horn,et al.  Generalization of learned preferences in filial imprinting , 1992, Animal Behaviour.

[61]  S. Cook Retention of primary preferences after secondary filial imprinting , 1993, Animal Behaviour.

[62]  W. Tryon Neural networks for behavior therapists: What they are and why they are important , 1995 .