G. Horn

PATHWAYS OF THE PAST: THE IMPRINT OF MEMORY

Memory is central to many aspects of behaviour, but in spite of a long interest in its neural basis, empirical evidence of the nature of the hypothetical pathway that is left in the vertebrate central nervous system by learning has been elusive. An important impediment has been the difficulty of localizing a brain region in which information is stored, but this difficulty has largely been overcome in the case of the learning process of visual imprinting. Most theories of memory suppose that an experience or event leads to the formation or strengthening of particular pathways in the brain. The evidence that is derived from imprinting partly supports this view, but the processes involved are more complex and more interesting than has been supposed.

Effects of restricted lesions of the chick forebrain on the acquisition of filial preferences during imprinting

The effects of placing bilateral lesions in that part of the chick brain (IMHV) which was previously been implicated in imprinting, was studied in young domestic chicks. Twenty-four dark-reared chicks were matched in pairs on the basis of their approach activity during a 30 min period of exposure to one of two visual imprinting stimuli. Both members of the chick pair were then anaesthetized and bilateral lesions were made by radio-frequency coagulation in the IMHV of one chick; the other chick served as a sham-operated control. On the following day each chick was exposed for 2.5 h to the imprinting stimulus to which it had previously been exposed. After training, the preferences of all chicks were measured by comparing their approach to the training stimulus with that to the second stimulus. Sham-operated chicks showed a strong preference for the training stimulus; lesioned chicks showed none. Subsequently the latency of each chick to approach and accurately peck a shiny rod was measured. The two groups of chicks did not differ significantly in this test of visuomotor coordination. The area of tissue damaged by the lesion was reconstructed: IMHV was severely damaged with relatively little damage to other areas of the brain.

Visual imprinting and the neural mechanisms of recognition memory

To understand the neural bases of memory it is necessary to localize the regions storing information. Part of the hyperstriatum ventrale (IMHV) serves such a function for the learning process of imprinting in domestic chicks. Chicks exposed to an object learn its characteristics, and in doing so, the responsiveness of IMHV neurones to that object is selectively enhanced. Imprinting is associated with both pre- and postsynaptic changes in the region. Postsynaptic changes involve increases in the length of the postsynaptic density on dendritic spines and in the numbers of NMDA receptors; presynaptically, converging evidence points to an early and persistent enhancement of neurotransmitter release. Increases in the amounts of certain neural cell adhesion molecules a day after training might serve to stabilize the synaptic changes associated with a particular memory by strengthening pre- to postsynaptic adhesion, and by more strongly interconnecting the cytoskeletal frameworks of the dendritic spine and the synaptic terminal. Learning-related increases in the number of neurones staining positive for the transcription factor Fos in the IMHV give promise of identifying the neurones engaged in memory functions and of analysing their connections.

Hemispheric asymmetry and imprinting: The effect of sequential lesions to the hyperstriatum ventrale

SummaryThe respective roles in the imprinting process of parts (IMHV) of the left and right hyperstriatum ventrale of the chick brain were examined by destroying first one and then the other IMHV in a two-stage operation. One hundred and eight chicks were dark-reared to ≃ 19 h post-hatch and exposed to a training stimulus for 2 h. Chicks were anaesthetised ≃ 3 h after the end of training. Lesions were placed in either (i) right IMHV (N = 18 birds), (ii) left IMHV (N = 18) or (iii) left or right hyperstriatum accessorium (HA; N = 18). Fifty-four chicks served as sham-operated controls. Chicks were returned to the dark incubator, and, 15–20 h after the operation, the chicks’ approach towards the training stimulus and to a second novel stimulus was measured (Test 1). After this test the chicks were again anaesthetised and a second lesion was made, this lesion being placed in the corresponding structure (IMHV or HA) of the hemisphere contralateral to that with the first lesion. The chicks’ preferences were measured 15–20 h later (Test 2). In Test 1, all birds strongly preferred the training stimulus. In Test 2, sham-operated controls and HA chicks continued to prefer the training stimulus as did chicks with the initial lesion in the left IMHV. However, chicks with the initial lesion in the right IMHV failed to show a preference for the training stimulus. Thus, if the right IMHV is destroyed first the presence of the left IMHV is crucial for retention. In contrast, if the left IMHV is destroyed first the presence of the right IMHV is not crucial for retention: chicks continue to prefer the training stimulus after the right IMHV has been lesioned. In these circumstances, therefore, some region outside IMHV takes on a memory function. The results imply that at least two memory systems are formed during imprinting. One of these involves the left IMHV, the other does not. The putative second system is fully able to sustain recall in the normal chicks by ≃ 26 h after training: if bilateral lesions to IMHV (N = 28 chicks) are made at this time, retention, measured 15–20 h later, is not significantly different from that of sham-operated control chicks (N = 25).

Development of filial preferences in dark-reared chicks

When given a simultaneous choice preference test 24h after being allowed a period of time in running wheels, dark-reared domestic chicks, Gallus gallus domesticus, will approach a stuffed jungle fowl in preference to a red box. The present study was designed to determine which aspects of the stuffed fowl were critical for the emergence of this preference. In all experiments the preferences of dark-reared chicks were studied in a test involving the simultaneous presentation of an intact stuffed jungle fowl and a second, test object. In experiment 1 this object was a ‘complex’ red box, in experiments 2.1 and 2.2 disarticulated stuffed fowl, and in experiment 2.3 the ‘scrambled’ skin of a jungle fowl. The results of these experiments suggested that particular arrangements or configurations of features, and not outline or textural complexity alone, are important for the emergence of the predisposition. Further support for this hypothesis was obtained in experiment 2.4 in which the intact fowl was compared to a test object containing such configurations of features. The result of experiment 3 suggested that the configuration of features associated with the head and neck region are particularly important, while the results of experiments 4 and 5, in which the test objects were a stuffed gadwall duck and a stuffed polecat, respectively, established that the configuration of features esential for the predisposition is not species specific.

Amnesic effects of bilateral lesions placed in the hyperstriatum ventrale of the chick after imprinting

SummaryThe purpose of this study was to investigate whether bilateral lesions to a part of the hyperstriatum ventrale (IMHV) impair retention if they are placed after chicks have been imprinted. Domestic chicks were hatched and reared in darkness and exposed to an imprinting (training) stimulus for 2 h commencing ≃ 22 h post hatch. The chicks were then anaesthetised and bilateral lesions placed in IMHV (N = 16) birds, hyperstriatum accessorium (HA; N = 16) or the lateral part of the cerebral hemispheres (LCA; N = 16). Forty-eight sham-operated chicks served as controls. Chicks were returned to the dark incubator, and, 15–20 h after the operation, their approach towards the training stimulus and to a second novel stimulus was measured. The controls and the chicks with lesions in HA and LCA showed a strong preference for the training stimulus and hence a high level of retention. The preferences of these three experimental groups did not differ significantly from one another. The mean preference of chicks with lesions in IMHV was significantly less than that of the sham-operated controls (P<0.01) and of chicks lesioned in HA (P<0.05). Bilateral lesions to IMHV therefore selectively impair retention of a preference acquired through imprinting. This impairment is unlikely to be a non-specific consequence of defective sensory processing or motor performance because the four groups did not differ from each other in (i) the time taken accurately to peck a rocking bead, (ii) the accuracy of pecking millet seeds and (iii) the performance of a simultaneous visual discrimination task involving heat reinforcement.

Receptive fields of units in the visual cortex of the cat in the presence and absence of bodily tilt

SummaryThe receptive fields of units in the visual cortex of anaesthetised cats were studied using spots or slits of light. Some fields were found to be stable when they were repeatedly plotted with the cat maintained in the horizontal position: other fields were not stable and the sharpness of spatial tuning varied though the orientation of the axis did not shift. When the cat was tilted the field axis of the majority of cells followed the tilt. In 14 cells, however, changes occurred in the receptive field which were not observed when the animal remained in the horizontal plane. These changes included drifts of the field axis in a direction which, with one exception, was opposite to the tilt, and alterations in the spatial extent of the field. On returning the animal to horizontal the axis of 4 fields drifted past the original orientation. These effects were not eliminated by either bilateral destruction of the labyrinth or high cervical transection of the spinal cord. The time of onset of the tilt effects varied from cell to cell: some of this variability is probably an effect of anaesthesia.The findings are consistent with the view that the receptive field of certain cells in the visual cortex are capable of being modified, one of the modifying influences being the orientation of the body in space.

Effects of early experience on regional incorporation of precursors into RNA and protein in the chick brain

Summary This study reports the effects of an imprinting procedure on the incorporation of radioactive lysine and radioactive uracil into acid-insoluble substances in the brains of 1-day-old domestic chicks. Experimental groups were exposed to a flashing light, light control groups to a constant overhead light, and dark control groups were kept in the dark at the same temperature as the other two groups. After 115 min of exposure the incorporation of lysine into presumed protein was significantly greater in the forebrain roof region of the early-hatching experimental group than the dark control group. After 160 min of exposure the forebrain regions of both experimental and light control groups showed a significantly greater incorporation of uracil into presumed RNA than did the forebrains of the dark control group. However, after 76 min incorporation of uracil into RNA was significantly enhanced only in the forebrain roof region of the experimental group. Specific effects of the imprinting procedure may emerge quite rapidly in the forebrain roof but are eventually overlain by non-specific effects of exposure to light.

Interaction between acquired preferences and developing predispositions during imprinting

Abstract Preferences of domestic chicks were studied either at approximately 2 h or approximately 24 h after exposure to a red box or a stuffed jungle fowl. Preferences of the chicks were measured in a simultaneous choice test involving these two stimuli. When tested at about 2 h, chicks preferred the object to which they had previously been exposed. Chicks tested at about 24 h showed a significantly greater preference for the jungle folw than those tested at about 2 h, regardless of the training stimulus. Birds that had been placed in a running wheel and exposed to diffuse light also showed an increasing preference for the fowl over time when tested in the same manner. These results may be accounted for in terms of an interaction between two processes, a developing predisposition for the fowl on the one hand and a preference acquired through learning on the other.

Monocular imprinting and regional incorporation of tritiated uracil into the brains of intact and "split-brain" chicks.

Abstract When intact chicks with a patch over one eye were exposed at a post-hatch age of 14–19 h to a flashing light, no regional differences between the two hemispheres were found in the incorporation of tritiated uracil into acid-insoluble residues. Similar biochemical studies were made using 12 chicks in which the supraoptic commissure had been transected. Each chick had one eye covered with a patch and was exposed to a flashing yellow light for a total of 60 min. It was subsequently given two choice tests between the familiar flashing yellow light and an unfamiliar flashing red light, first with its trained eye alone exposed and then with its untrained eye alone exposed. All of the 12 chicks approached the familiar flashing yellow light with the originally trained eye uncovered, but not with the originally untrained eye uncovered. The rate of incorporation of tritiated uracil into presumed RNA was 15.2% higher in the trained side of the forebrain roof than in the untrained side. No other regional differences between trained and untrained sides were observed. The results show that certain non-specific consequences of the imprinting procedure, such as general changes in hormonal levels as a result of stress, non-visual sensory stimulation and motor activity, cannot account for the observed biochemical changes in the forebrain roof.