Memory in the chick: Multiple cues, distinct brain locations.

Training chicks on a 1-trial passive avoidance task results in memory-dependent synaptic remodeling in the intermediate medial hyperstriatum ventrale (IMHV) and lobus parolfactorius (LPO). Because pretraining IMHV lesions are amnestic and posttraining IMHV lesions are not, the functional significance of this remodeling requires explanation. Chicks use various cues to classify and remember objects. If the IMHV were concerned with memory for only one such cue, then posttraining IMHV lesions would not lead to "amnesia" because animals would still avoid the aversive bead using other contextual cues. This hypothesis was tested using a color discrimination task. IMHV lesions, but not LPO lesions, impair color discrimination, suggesting that the IMHV may be involved in classifying and remembering the bitter bead on the basis of color. Thus, even simple associations are stored in the brain in the form of multiple, dispersed representations. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Passive avoidance training and recall are associated with increased glutamate levels in the intermediate medial hyperstriatum ventrale of the day-old chick

In the young chick, the intermediate medial hyperstriatum ventrale is involved in learning paradigms, including imprinting and passive avoidance learning. Biochemical changes in the intermediate medial hyperstriatum ventrale following learning include an up-regulation of amino-acid transmitter levels and receptor activity. To follow the changes of extracellular amino acid levels during passive avoidance training, we used an in vivo microdialysis technique. Probes were implanted in chicks before training the animals, either on a methylanthranylate- or water-coated bead. One hour later, recall was tested in both groups by presenting a similar bead. An increase of extracellular glutamate levels accompanied training and testing in both groups; during training, glutamate release was higher in methylanthranylate-trained than in water-trained chicks. When compared with the methylanthranylate-trained chicks during testing, the water-trained chicks showed enhanced extra-cellular glutamate levels. No other amino acid examined showed significant changes. After testing, the chicks were anesthetized and release-stimulated with an infusion of 50 mM potassium. Extracellular glutamate and taurine levels were significantly increased in both methylanthranylate- and water-trained chicks. The presentation of methylanthranylate as an olfactory stimulus significantly enhanced glutamate levels, especially in methylanthranylate-trained chicks. The results suggest that such changes in extracellular glutamate levels in the intermediate medial hyperstriatum ventrale accompany pecking at either the water- or the methylanthranylate-bead. The taste of the aversant may be responsible for the greater increases found in methylanthranylate-trained birds.     

Passive avoidance learning involves alpha2-noradrenergic receptors in a day old chick

Day-old chicks were trained on one-trial passive avoidance task, using methyl-anthranilate (MeA) as an aversive substance. Bilateral pharmacological manipulation of the intermediate hyperstriatum ventrale was performed by intracerebral application of an alpha2-noradrenergic agonist, clonidine (5 microM), or an antagonist, rauwolscine (300 microM). Only rauwolscine application (pre- or post-training) induced significant memory impairment. Quantitative receptor autoradiography was used to determine the kinetic properties of the binding sites for [3H]clonidine or [3H]rauwolscine in MeA-trained or water-trained (control) chicks, in forebrain areas known to be involved in avoidance learning. Scatchard analysis revealed that MeA-training resulted in a significant bilateral upregulation in the number of [3H]rauwolscine binding sites (Bmax) in the area of hyperstriatum ventrale. These findings suggest the importance of activation of alpha2-noradrenergic receptors in aversive learning in chicks.     

Neural cell adhesion molecules, learning, and memory in the domestic chick

The intermediate and medial hyperstriatum ventrale (IMHV) of the chick forebrain is a site of recognition memory for the learning process of imprinting. The results reported here demonstrate that neural cell adhesion molecules (NCAMs) play a time-dependent role in this recognition memory. Dark-reared chicks were trained, tested, and assigned a preference score as a measure of learning. Chicks with high preference scores were designated good learners and those with lower preference scores, poor learners. Controls were untrained. Tissue was removed, 9.5 hr or 24 hr after training, from the left and right IMHV, hyperstriatum accessorium, and posterior neostriatum. Three major NCAM isoforms (180, 140, and 120 kDa) were assayed. At 24 hr only, there was in left IMHV significantly more NCAM (for each isoform) in good learners than in the other 2 groups, and also a significant correlation between the amounts of NCAM and preference scores for all isoforms; the amount predicted by each regression line at preference score 50 (no learning) did not differ significantly from the mean value for untrained controls. There were no learning-related effects in either the hyperstriatum accessorium or the posterior neostriatum.     

Impairment of learning by localized injection of an N-methyl-D-aspartate receptor antagonist into the hyperstriatum ventrale of the domestic chick.

A restricted part of the domestic chick forebrain is critically involved in the learning process of imprinting. This region is the intermediate and medial part of the hyperstriatum ventrale (IMHV). The effect on imprinting of local injection of the N-methyl-{d}-aspartate (NMDA) receptor blocker {d}-amino-5-phosphonopentanoic acid ({d}-AP5) into the left IMHV was studied in chicks in which the right IMHV had been lesioned. The left IMHV is essential for imprinting when chicks have been lesioned in this way. Injection of ～0.7 nmol {d}-AP5 into the left IMHV significantly impaired imprinting. Injection of ～0.2 nmol {d}-AP5 into the left IMHV, or of ～0.7 nmol {d}-AP5 into the left hyperstriatum accessorium, was without significant effect on imprinting. These results suggest that NMDA receptors in the left IMHV may play an important part in this learning process. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Lateral hyperstriatal lesions disrupt simultaneous but not successive conditional discrimination learning of pigeons (Columba livia).

Explored, in 2 experiments, the effects of lateral vs medial laminar lesions of the hyperstriatum in pigeons; medial lesions were largely confined to the hyperstriatum accessorium, and lateral lesions to the hyperstriatum dorsale and hyperstriatum ventrale. In Exp 1, lateral, but not medial, lesions disrupted acquisition of a simultaneous conditional discrimination; both medial and lateral lesions disrupted reversal of the discrimination. The reversal deficits of the medial and lateral groups were quantitatively similar, and both groups showed exaggerated positional responding. In Exp 2, neither medial nor lateral lesions disrupted acquisition of a successive conditional discrimination. Lateral hyperstriatal damage does not obtain a general disruption of conditional learning; it is speculated that the lateral hyperstriatum may play a critical role in configural learning. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Distinct activation of monoaminergic pathways in chick brain in relation to auditory imprinting and stressful situations: a microdialysis study

In the forebrain of the domestic chick (Gallus gallus domesticus), an area termed the mediorostral neostriatum/hyperstriatum ventrale is strongly involved in emotional learning paradigms such as acoustic filial imprinting. Furthermore, the involvement of the mediorostral neostriatum/hyperstriatum ventrale in stressful situations, such as social separation, has been demonstrated in 2-deoxyglucose studies. The aim of the present study was to examine whether quantitative changes of dopamine, serotonin and their metabolites occur during auditory filial imprinting and during social separation. Using in vivo microdialysis in tone-imprinted and in naive, control chicks, we compared the extracellular levels of homovanillic acid, a metabolite of dopamine, and 5-hydroxyindoleacetic acid, a metabolite of serotonin, during the presentation of the imprinting tone. A small, but statistically significant, decrease of extracellular homovanillic acid levels was found in the mediorostral neostriatum/hyperstriatum ventrale of imprinted chicks compared to control animals, whereas changes of 5-hydroxyindoleacetic acid were not detected. In a second experiment, we investigated the levels of homovanillic acid and 5-hydroxyindoleacetic acid in the mediorostral neostriatum/hyperstriatum ventrale of socially reared chicks during different stress situations, such as handling or separation from their cage mates. Handling induced a significant increase of homovanillic acid and 5-hydroxyindoleacetic acid, while social separation resulted in a significant increase of 5-hydroxyindoleacetic acid and only a slight increase of homovanillic acid. Despite considerable inter-individual variability, the increase of distress vocalizations (duration of distress calls) after social separation displayed a good correlation to the increased 5-hydroxyindoleacetic acid levels in all animals analysed. These results provide the first evidence that the physiological response of the mediorostral neostriatum/hyperstriatum ventrale related to different emotional conditions after acoustic imprinting and during stressful situations is, at least in part, mediated by dopaminergic and/or serotonergic pathways. Furthermore, the results from the present study indicate a distinct activation of dopaminergic and serotonergic pathways in relation to the behavioural situation and the associated changes of emotional status.     

Functionally distinct memories for imprinting stimuli: Behavioral and neural dissociations.

Precocial chicks exposed to a stimulus subsequently approach that stimulus in preference to other, novel stimuli. Previous investigations of the neural basis of these imprinting preferences suggest that imprinting training results in the formation of two memories. The first memory is formed rapidly and is located in the intermediate and medial part of the hyperstriatum ventrale (IMHV) of the left hemisphere; the formation of the second, in another memory system, S', takes several hours and can be prevented by a lesion placed in the right IMHV soon after training. The results of the present study suggest that the functional characteristics of these memories differ. Although memories in both left IMHV and S' supported imprinting preferences (Experiments 1a and 2a), only memories in S' influenced the acquisition of a heat-reinforced discrimination in which imprinted objects served as discriminanda (Experiments 1b and 2b). (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Effects of light hatching on synapse number and size in the intermediate and medial part of the hyperstriatum ventrale of the domestic chick

The effects of pre-hatch light exposure on synaptic development in the intermediate and medial part of the hyperstriatum ventrale (IMHV) of the chick brain were investigated. Quantitative electron microscopical techniques were used to determine the size and numerical density of synapses and it was seen that in light hatched chicks there was a significant increase in the density of synapses in the left IMHV but that the size of synapses in these birds was decreased. These results provide a link between synaptic development and plasticity.     

Noradrenaline and learning: Effects of the noradrenergic neurotoxin DSP4 on imprinting in the domestic chick.

In 2 experiments, 168 domestic chicks received intraperitoneal injections of 50 mg/kg of N-(2-chlorethyl)-N-ethyl-2-bromobenzylamine HCl (DSP4) or distilled water and were trained 60 hrs after hatching by exposing them to either a rotating red box or a stuffed jungle fowl. Noradrenaline concentration was determined in Wulst and medial and basal forebrain samples. The medial forebrain sample comprised mainly the intermediate part of the medial hyperstriatum ventrale, a region previously shown to be involved in imprinting. DSP4 treatment reduced forebrain noradrenaline levels by about 65% and also profoundly impaired imprinting in box-trained but not fowl-trained Ss. In box-trained Ss, the strength of imprinting was positively correlated with noradrenaline concentration in both medial and basal forebrain samples. It is suggested that some of the neural structures and mechanisms involved in imprinting on the fowl differ from those involved in imprinting on the box. (43 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Encoding of geometric and landmark information in the left and right hemispheres of the avian brain.

Chicks were trained binocularly to find food buried under sawdust in the center of a square enclosure. When tested in an enclosure made larger or smaller in size, binocular and left-eyed chicks searched mainly on the basis of relative distance of the food from the enclosure walls, whereas right-eyed chicks searched on the basis of absolute distance. Moreover, binocular and left-eyed chicks relied mainly on global spatial information (i.e., distances from the walls), whereas right-eyed chicks also used information provided by visual landmarks. These results suggest that the right hemisphere of the avian brain (fed mostly by the left eye) is primarily concerned with encoding of relational spatial information, whereas the left hemisphere (fed mainly by the right eye) is concerned with absolute metric information, possibly as part of an encoding strategy based primarily on local (both spatial and nonspatial) cues. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Influence of opioid peptides on learning and memory processes in the chick.

Several experiments were conducted to examine the effects of intracranial injection of opioid peptides and antagonists on learning and memory in the chick. Pretraining injection of [leu–5]enkephalin and the selective delta receptor agonist [D-Pen–2,L-Pen–5]enkephalin (DPLPE) into the intermediate medial hyperstriatum ventrale (IMHV) produced impairment. ICI 174,864, a delta-selective antagonist, reversed the impairment produced by either [leu–5]enkephalin or DPLPE, results indicating that delta receptors may play a role in learning in the chick and suggesting that the impairment produced by [leu–5]enkephalin is mediated through delta opioid receptors. β-endorphin produced a naloxone-reversible impairment in performance, which suggests that this impairment is mediated by opioid receptors. Bilateral injection of β-endorphin into the IMHV produced impairment, as did unilateral injection into the right, but not left, IMHV. Only bilateral injections into IMHV of [leu–5]enkephalin were effective. These results suggest that the effects of β-endorphin are centrally mediated whereas the effects of [leu–5]enkephalin may be localized to other brain regions or are peripherally mediated. These initial results suggest that opioids are associated with learning and memory in the chick. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Unilateral injury of posterior parietal cortex and spatial learning in hooded rats

The influences of bilateral or unilateral injuries within the posterior parietal cortex (PPC) upon spatial learning in a water maze were examined in three experiments. Place-learning and response-learning were investigated in a four-alley 'Greek-cross' shaped water maze with extra-maze visual cues available. No differences were detected on any of several measures sensitive to learning between the lesion groups on the place-learning task. Microanalysis of behavior within trials revealed that animals with either bilateral or right unilateral PPC injuries committed significantly more total errors, initial alley entrance ('reference memory') errors, and re-entry ('working memory') errors in the response-learning paradigm than did either the control or left PPC-injured rats. No differences were detected between the latter two groups on these measures. Unilateral lesions resulted in asymmetrical placing responses ipsilateral to the injury 10 days after surgery whereas bilateral injuries resulted in asymmetrical placing with mixed directionality. The acquisition of the response-learning problem in the absence of visual cues was studied on animals prepared with unilateral lesions and housed post-operatively either in isolation or in a 'complex environment.' In the absence of visual cues both right and left PPC-injured rats committed more errors than sham controls, and differential post-surgical housing did not attenuate these impairments. These same animals were trained on the landmark navigation task. Although no differences appeared between the lesion groups, a generalized but transient facilitation of learning was observed in animals housed in the 'complex' environment. Unilateral injuries placed in sham controls failed to disturb retention of the landmark navigation strategy. Because none of the PPC-injured animals were deficient in the landmark task, a result which is contrary to observations in other laboratories, the influence of post-surgical recovery interval upon acquisition of the landmark navigation strategy was explored. Animals were prepared with right PPC injuries and trained following either a 5 or 35 day recovery interval. Only those animals limited to the short recovery interval proved to have a spatial deficit in the landmark task. It is concluded that injuries in the PPC of either hemisphere disturb egocentric spatial functions. However, animals with left PPC injuries are able to compensate by using allocentric visual cues if they are available. It is due to the special role played by the right PPC in complex visuospatial functions that animals with this injury are unable to compensate.     

Learning selectively increases protein kinase C substrate phosphorylation in specific regions of the chick brain

The effect of imprinting, an early form of exposure learning, on the phosphorylation state of the protein kinase C substrates myristoylated alanine-rich C-kinase substrate (MARCKS) and protein F1/43-kDa growth-associated protein (F1/GAP-43) was studied in two regions of the chick forebrain. One region, the intermediate and medial part of the hyperstriatum ventrale (IMHV), is probably a site of long-term memory; the other, the wulst, contains somatic sensory and visual projection areas. After imprinting, a significant increase in MARCKS protein phosphorylation was observed in the left IMHV but not the right IMHV. No significant alteration in F1/GAP-43 was observed in IMHV. MARCKS was resolved into two acidic components of pI approximately 5.0 and approximately 4.0. Phosphorylation of the pI approximately 5.0 MARCKS but not the pI approximately 4.0 MARCKS was significantly altered by imprinting. The partial correlation between preference score (an index of learning) and phosphorylation, holding constant the effect of approach activity during training, was significant only for the pI approximately 5.0 MARCKS in the left IMHV. A significant negative partial correlation between preference score and F1/GAP-43 phosphorylation in the right wulst was observed. Because the imprinting-induced alteration in MARCKS is selective with respect to phosphoprotein moiety, hemispheric location, and brain region, we propose that these alterations may be central to the learning process.     

Protein kinase C inhibitor chelerythrine disrupts memory formation in chicks.

Chelerythrine (CHELE), a specific, potent protein kinase C (PKC) inhibitor, disrupts memory formation for a one-trial peck-avoidance task. Three predictions were made about how CHELE, injected into chick brain near the time of training, would affect memory formation, based on previous work with two classes of protein kinase inhibitors (M. R. Rosenzweig et al, 1992; P. A. Serrano et al, see record 1994-20797-001) and the in vitro inhibition of PKC by CHELE: (1) CHELE, injected into the intermediate medial hyperstriatum ventrale, would significantly impair memory formation; (2) the amnestic dose would be approximately 10 nmol; (3) CHELE would not produce amnesia for about 45 min after training, but significantly impair memory by 60 min. Experimental tests confirmed each prediction. This study adds to evidence that PKC activity is part of a cascade of neurochemical events initiated by learning and that PKC activity shortly after training is necessary for long-term memory. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Reversal learning in pigeons: Effects of selective lesions of the Wulst.

Evaluated the effects of bilateral lesions of individual laminae of the Wulst on reversal-learning performance in pigeons. After surgery, Ss were trained to perform a simultaneous color discrimination. Once successful discrimination was achieved, the positive and negative stimuli were reversed, and Ss were again trained to criterion. 20 reversals were carried out. A multiple regression analysis indicated that those components of the Wulst that were critical for increasing the numbers of errors on each reversal were the laminae that receive the thalamofugal visual projections (i.e., the nucleus intercalatus of the hyperstriatum accessorium and the hyperstriatum dorsale). Lesions in the other laminae of the Wulst (the hyperstriatum accessorium and the hyperstriatum intercalatus superior) had no effect on errors. There was no evidence of an increase in either perseverative errors or position habits in the Ss with lesions, suggesting that the reversal deficits were not likely to be due to perseveration, attentional impairment, or inappropriate processing of spatial information. The deficit may have been produced by excessive interference between learning in a given session and learning in previous sessions. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Effects of substantia nigra and caudate nucleus lesions on avoidance learning in rats.

Compared to 21 operated and 14 nonoperated controls, 36 male Sprague-Dawley albino rats with small bilateral lesions in the anteroventral caudate nucleus or the rostral substantia nigra were significantly impaired in the acquisition of 1-way active avoidance, passive avoidance requiring the inhibition of the previously acquired 1-way response, and shuttle-box avoidance. Ss with nigral lesions took significantly more trials to criterion than Ss with caudate lesions on 1-way avoidance. Results are considered in terms of the intimate anatomical and neurochemical relationships between these structures, and a circuit of structures involved in avoidance learning is suggested. (34 ref.) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Deficient passive and one-way active avoidance acquisition following medial forebrain bundle lesions in rats.

In 3 experiments with 93 Long-Evans male hooded rats, cathodal electrolytic lesions of the medial forebrain bundle (MFB) at posterior hypothalamic levels produced a mild, transient hypodipsia and lowered jump thresholds to footshock. Lesions produced marked deficits in passive avoidance performance in a paradigm that paired discrete, linearly incrementing footshock intensities with contact of a water spout following 48 hrs of water deprivation. Injections of levo-dextro-5-hydroxytryptophan (75 mg g, ip), the immediate metabolic precursor of serotonin, had no effect on the passive avoidance performance of either experimental or operated control Ss. Lesions of the MFB also resulted in deficient acquisition in a 1-trial step-through passive avoidance paradigm not using motivation to drink and caused a severe acquisition deficit in a 1-way active avoidance task. Lesions of the septal nuclei produced lowered jump thresholds but did not affect acquisition in the 1st passive avoidance task. Results are interpreted as indicating a lesion-induced deficiency in fear learning, independent of the serotonergic functions of the MFB. (45 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Differential recovery of function following caudate, hippocampal, and septal lesions in mice.

Tested female CF1 mice with bilateral caudate, hippocampal, or septal lesions for passive avoidance learning at 1-2, 7-8, or 28-29 days after surgery. Although each lesion induced a comparable learning impairment at 1-2 days after surgery, time-dependent recovery occurred only with caudate lesions. Each lesion also induced changes in sensitivity to dextroamphetamine and scopolamine at 1-2 days after surgery, and further time-dependent variations in drug sensitivity occurred only with caudate lesions. Results suggest that normal acquisition of passive avoidance behavior is mediated by a critical septal-hippocampal system and another, perhaps redundant, system involving the caudate. Time-dependent drug sensitivity changes following caudate lesions were consistent with a role of denervation supersensitivity in recovery of function. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Salbutamol overcomes the effect of the noradrenergic neurotoxin DSP-4 on memory function in the day-old chick

These experiments investigated the effect of the relatively selective noradrenergic neurotoxin N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine (DSP-4) on memory formation in day-old chicks trained on a discriminated passive avoidance task. A time course study showed that DSP-4 treatment resulted in amnesia as early as 20 min post-learning. In a second study, a series of alpha- and beta-adrenergic agonists (noradrenaline; the alpha 1 agonist phenylephrine; the beta 1 agonist dobutamine; and the beta 2 agonist salbutamol) were applied immediately after the training trial. Both noradrenaline and salbutamol were effective in ameliorating the memory deficits caused by DSP-4 treatment, and in consolidating weakly reinforced training. These studies support the notion that noradrenaline subserves a vital role in the consolidation of memory in the chick, and that the beta 2 receptor subtypes are principally involved in the intermediate phase of memory formation.