European Journal zyxwvutsrq of Neuroscience, Vol. 6, pp. zyxwvutsrq 1479-1490, 1994 zyxwvu 0 European Neuroscience Association z Learning-related Alterations in the Visual Responsiveness of Neurons in a Memory System of the Chick Brain M. W. Brown and G. Horn' Department of Anatomy, School of Medical Sciences, University of Bristol, Bristol BS8 lTD, UK 'Department of Zoology, Downing Street, University of Cambridge, Cambridge CB2 3EJ, UK Key words: imprinting, recognition memory, IMHV, sensory responses, neuronal activity Abstract The intermediate and medial hyperstriatum ventrale (IMHV) of the chick brain is known to be essential for the learning process of imprinting. The activity of neurons was recorded from the left IMHV of 2-day-old unanaesthetized chicks while the chicks were free to move in a running wheel. The chicks were either raised in complete darkness or visually trained (imprinted) with a set duration of exposure to a visual image. The first group of these birds was trained by exposure for 100 min to a rotating red box and the second was trained by similar exposure to a rotating blue cylinder. A third group was left untrained. Training more than doubled the proportion of sites that responded to the stimulus used to train the bird, relative to the proportion of sites responsive to the other stimulus and to the proportion of sites responsive in the untrained birds; the learning- related increase was selective and highly significant. Behavioural monitoring indicated that the enhanced responsiveness could not be explained by overt differences in the alertness, attentiveness or movements of the birds. No significant effect of training was found on the proportion of sites responsive to a rotating stuffed jungle fowl or to the sound of a maternal call. The response at certain sites selectively signalled the presence of the training stimulus, while at others the response showed generalization across stimulus shape or colour. There was a nonspecific effect of training upon the pattern of spontaneous discharges of the neurons: the numbers of spikes occurring in clusters (bursts) was significantly reduced in trained birds compared with the dark reared controls. Introduction zyxwvutsrqpo Imprinting is the process by which the young of some species, including the domestic chick, learn the characteristics of an zyxwvuts object by being exposed to it (for review see Bolhuis, 1991). Visually naive chicks initially approach a wide range of objects, but if they are exposed to one of them for - 1 h they selectively approach it: when chicks which have been trained in this way are given a choice between the object to which they have been exposed and another object, they preferentially approach the training object. When zyxwvutsrq this object is absent the chicks tend to emit distress calls and when the object is present the chicks tend to emit contentment calls. This pattern of behaviour provides the evidence that the chicks recognize, and hence have a memory of, the training object. zyxwvuts A restricted part of the chick telencephalon is involved in this memory process (for reviews see Horn, 1985, 1990, 1991). The region is the intermediate and medial part of the hyperstriatum ventrale zyxwvutsr (MHV). Briefly, the evidence for this involvement is that after imprinting there is in this region: (i) an increased incorporation of [L4C]uracil into RNA - this increase was not found in any other brain region studied (Horn et al., 1979); (ii) within 1 h after training, an increase in the expression of the immediate early gene product Fos (Ambalavanar et al., 1993; McCabe and Horn, 1993, 1994; (iii) an increase in the length of the postsynaptic density of axospinous synapses - these changes were not found in a visual projection area, the hyperstriatum acceswrium (Bradley et al., 1981; Horn er al., 1985); (iv) an increase in N-methyl-maspanate (IWDA) receptor binding (McCabe and Horn, 1988,1991); (v) a change in the synthesis of proteins with molecular mass of 80 and 50 kDa in the left IMHV but not in two other regions of the left cerebral hemisphere (Brown and Horn, 1990); and (vi) an increase in endogenous phosphorylation of a protein kinase C substrate protein (Sheu et al., 1993). The changes referred to in (iii), (iv) and (vi) were observed in the left but not the right IMHV. Further, the changes referred to in (ii), (iv) and (vi) were significantly correlated with a measure of how much the chicks had learned about the visual imprinting object and could not be accounted for in terms of light exposure, arod or locomotor activity. Bilateral destruction of the IMHV impaired the acquisition and retention of an imprinted preference (McCabe et al., 1981,1982; Takamatsu and Tsukada, 1985). Studies of lesions placed sequentially in the left or the right IMHV suggest that both regions may be sites of information storage (Cipolla-Net0 et al., 1982; Horn er al., 1983), though the two sides may have different roles in memory function. The IMHV is c o~~ted to the visual pathways (Bradley er al., 1985; for review see Horn, 1985, pp. 233-235 and fig. 11.1). It might therefore be anticipated that neurons in the IMHV would be responsive Correspondence to: M. W. Brown, as above; zyxwvutsrq email: M.W.Brown@uk.ac.bristol Received 5 January 1994, revised 19 April 1994, accepted 20 April 1994