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Modeling the Dishabituation Hierarchy: the Role of the Primordial Hippocampus*

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Modeling the Dishabituation Hierarchy: the Role of the Primordial Hippocampus* Biol. Cybern. 67, 535-544 (1992) Biological Cybemetics Springer-Verlag 1992 Modeling the dishabituation hierarchy: The role of the primordial hippocampus* DeLiang Wang and Michael A. Arbib Center for Neural Engineering, University of Southern California, Los Angeles, CA 90089-2520, USA Received January 30, 1992/accepted in revised form April 6, 1992 Abstract. We present a neural model for the organiza- orienting response to a certain stimulus applied at a tion and neural dynamics of the medial pallium, the given location, the response can be released by the same toad's homolog of mammalian hippocampus. A neural stimulus applied at a different retinal locus (Eikmanns mechanism, called cumulative shrinking, is proposed 1955; Ewert and Ingle 1971). (2) Hierarchical stimulus for mapping temporal responses from the anterior tha- specificity. Another stimulus given at the same locus lamus into a form of population coding referenced by may restore the response habituated by a previous spatial positions. Synaptic plasticity is modeled as an stimulus. Only certain stimuli can dishabituate a previ- interaction of two dynamic processes which simulates ously habituated response. Ewert and Kehl (1978) acquisition and both short-term and long-term forget- demonstrated that this dishabituation forms a hierarchy ting. The structure of the medial pallium model plus the (Fig. 1A), where a stimulus can dishabituate the habitu- plasticity model allows us to provide an account of the ated responses of another stimulus if the latter is lower neural mechanisms of habituation and dishabituation. in the hierarchy. Computer simulations demonstrate a remarkable match A model developed by Wang and Arbib (1991a) between the model performance and the original exper- showed how a group of cells in the anterior thalamus imental data on which the dishabituation hierarchy was (AT) could respond to stimuli higher in the hierarchy based. A set of model predictions is presented, concern- with larger AT responses. The present paper studies ing mechanisms of habituation and cellular organiza- where and how the response activities are stored, and tion of the medial pallium. investigates the learning mechanisms involved in habit- uation and dishabituation. In addition to locus and hierarchical stimulus spe- cificity, prey-catching behavior in toads exhibits the 1 Biological basis following typical properties of habituation (for a review see Ewert 1984). Habituation is a decrease in the strength of a behavioral After the same prey dummy is presented at the response that occurs when an initially novel stimulus is same retinal locus repetitively, the response intensity presented repeatedly. It is probably the most elemen- decreases exponentially. tary and ubiquitous form of plasticity, and its underly- Spontaneous recovery occurs after the stimulus is ing mechanisms may well provide bases for withheld. The time course of recovery from habituation understanding other forms of plasticity and more com- exhibits two phases: a short-term process that lasts for plex learning behaviors. Amphibia show stimulus spe- a few minutes, and a long-term process which lasts for cific habituation. After repeated presentation of the at least 6 h. same prey dummy in their visual field, toads reduce the Habituation is faster and lasts longer with an strength of orienting repsonses toward the moving stim- increase in the number of training series. ulus. This visual habituation has the following charac- The response to the dishabituating stimulus de- teristics: (I) Locus specificity. After habituation of an creases with repeated presentation. The decrease of the response to a repeated dishabituating stimulus also follows a typical course of habituation. * The research described in this paper was supported in part by grant Dishabituation does not counteract the effects of no. IRO1 NS 24926 from the National Institutes of Health (M.A.A., previous habituation, but rather establishes a separate Principal Investigator) neuronal process (Wang and Ewert 1992). Correspondence to: D. Wang, Department of Computer and Informa- tion Science, Ohio State University, 2036 Neil Avenue Mall, Colum- Ceils with adaptation properties can be found in bus, OH 43210-1277, USA different visual neural structures. However, in retinal, 536 A receptive fields. After bilateral lesions of MP, toads showed no progressive decrease of the orienting activity 5m to repetitive stimulation (Finkenst/idt and Ewert 20~ 1988a). In addition, both effects of conditioning and ~ ~.~ mm''- associative learning ability in naive toads are abolished due to MP-lesions (Finkenst/idt and Ewert 1988b; Finkenst/idt 1989b). 1 * Lara and Arbib (1985), in their computational n - ,dL2 model, postulate that habituation is coded in telen- cephalic neurons which receive input from the tectum and modulate prey-catching behavior through their projection to TP neurons, which inhibit pyramidal neu- rons in the tectum, thus modulating the toad's orienting response. Their modeling of habituation processes fol- lows the general idea of the comparator model of stimulus-specific habituation (Sokolov 1960). However, movement g direct projections from the tectum to the telencephalon direction lack anatomical support. Furthermore, their assump- IIIIII tion of telencephalic modulation via TP is not consis- tent with the 2DG-uptake data that TP shows no change while the tectum shows a strong decrease after long-term habituation training (Finkenst/idt and Ewert 1988a). Ewert (1987) proposes the idea of neural loop inter- action to explain amphibian prey-catching behavior and its modulation (Fig. 1B). Loop (1) involves the tectum, the lateral anterior thalamic nucleus (La), the striatum, and the TP area, and is supposed to mediate prey- ,3 catching behavior; the so-called loop (2) starts with the retina and the tectum which send axons to AT and from there to MP, which then projects descendingly to PO and from there to HYP which in turn sends efferents to the tectum (retina ~ rectum --* A T ~ MP PO--*HYP ~ tectum). Loop (2) is supposed to modu- kEY late prey-catching behavior initiated in the tectum. All data obtained to date strongly suggest that MP is the Fig. 1. A Dishabituation hierarchy for worm stimuli in stimulus-spe- neural structure where learning occurs. For stimulus cific habituation. One stimulus can dishabituate all the stimuli below it. On the same level the left stimulus can slightly dishabituate the specific habituation in anurans, MP modulates prey- right one (redrawn with permission from Ewert and Kehl 1978). B catching behavior via the PO/HYP pathway, inhibiting Two neural loops mediating and modulating prey-catching behaviors tectal activities (Ewert 1987; Finkenst/idt and Ewert in toads. Abbreviations are: R: retina; OT: optic tectum; TP: thala- 1988a). Having modeled AT in Wang and Arbib mic-pretectal area; PO: preoptic region; HY: hypothalamus; AT: anterior thalamus; La: lateral anterior thalamic nucleus; MP medial (1991a), we now turn to a model of MP which com- pallium; and STR: striatum pletes our explanation of hierarchical dishabituation. tectal or TP (thalamic-pretectal) neurons, neither neu- 2 A neural model of the medial pallium ronal adaptation nor facilitation effects lasted longer than 90 to 120 s. Since behavioral studies show that Preliminary anatomical studies of the medial pallium habituation effects may last 24 h or longer, habituation indicate that this structure is organized in an orientation substrates must be located elsewhere. Anatomically, the vertical to the telencephalic ventricle, with cells mainly medial pallium (MP) has been thought to be a homolog projecting in this direction (Hoffman 1963; Kicliter and of the mammalian hippocampus ("primordium Ebbesson 1976). This leads us to suggest that the medial hippocampi" by Herrick 1933). Its location in the dor- pallium processes information by means of functional somedial wall of the hemisphere is in a position similar units, in a form of vertical columns, consistent with the to that of the mammalian hippocampal region. Finken- locus specificity of habituation in toad's prey-catching st/idt (1989a) identified three types of visual sensitive behavior. In what follows, we will model only one such neurons in MP which exhibit spontaneous firing activi- functional unit to demonstrate most of the properties of ties. MP1 neurons strongly increase, MP3 neurons de- hierarchical stimulus-specific habituation. crease, and MP2 neurons do not alter their discharge For stimulus-specific habituation, the medial pal- rates in response to 30 min of repetitive stimulation lium receives inputs from the anterior thalamus, a cell with a visual moving object traversing their excitatory type of which has been modeled in Wang and Arbib 537 (1991a). In the model, an MP column receives input ent positions in a subsequent array (Wang and King from an AT neuron, representing a specific visual loca- 1988; Wang and Arbib 1991b). The layers P1 and MP2 tion. The MP column model includes arrays of five together transform different temporal activities into types of neurons, MP1, MP2, and MP3 (Finkenst/idt spatial activity distribution centered at different posi- 1989a) and hypothetical cell types P1 and P2 (Fig. 2). tions. Suppose that each layer in the column has n P1 receives projections from AT, and projects to MP2. neurons, with mp~(i, t) the membrane potential of the MP2 projects to P2 and MP3. MP3 inhibits MP1, ith P1 cell, Ply, which further inhibits P2. The final outcome of the dmp,(i, t) functional column is reflected by a hypothetical neuron dt = -Aptmp,(i, t) + Bp,I(t) +0 (1) OUT that integrates activities from the P2 layer. The connections from MP2 to P2 and MP3 are the only where Apl is a relaxation parameter, and Bp~ is a plastic connections, that is, their efficacies are modifia- connection weight from the AT input, I(t), which is ble by training, which underlies stimulus-specific habit- assumed to be constant during a stimulus presentation. uation. For modeling simplicity, we assume that during 0 represents the amplitude of an uncorrelated white presentation of a given stimulus, a stable activity of noise term introduced to the AT input.
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