Johan J. Bolhuis

MECHANISMS OF AVIAN IMPRINTING: A REVIEW

Filial imprinting is the process through which early social preferences become restricted to a particular object or class of objects. Evidence is presented showing that filial preferences are formed not only as a result of learning through exposure to an object, but also under the influence of visual and auditory predispositions. The development of these predispositions is dependent upon certain non‐specific experience.

Evolution, brain, and the nature of language

Language serves as a cornerstone for human cognition, yet much about its evolution remains puzzling. Recent research on this question parallels Darwins attempt to explain both the unity of all species and their diversity. What has emerged from this research is that the unified nature of human language arises from a shared, species-specific computational ability. This ability has identifiable correlates in the brain and has remained fixed since the origin of language approximately 100 thousand years ago. Although songbirds share with humans a vocal imitation learning ability, with a similar underlying neural organization, language is uniquely human.

An Analysis of the Neural Representation of Birdsong Memory

Songbirds, such as zebra finches, learn their song from a tutor early in life. Forebrain nuclei in the “song system” are important for the acquisition and production of song. Brain regions [including the caudomedial part of the neostriatum (NCM) and of the hyperstriatum ventrale (CMHV)] outside the song system show increased neuronal activation, measured as expression of immediate early genes (IEGs), when zebra finch males are exposed to song. IEG expression in the NCM in response to tutor song is significantly positively correlated with the strength of song learning (i.e., the number of elements copied). Here, we exposed three groups of adult zebra finch males to tutor song, to their own song, or to novel conspecific song. The two control groups were included to examine an alternative explanation of our previous results in terms of variation in predisposed levels of attentiveness. Expression of Zenk, the protein product of the IEG ZENK, was measured in the NCM, CMHV, and hippocampus. There were no significant differences in overall Zenk expression between the three experimental groups. However, there was a significant positive correlation between Zenk expression in the NCM (but not in the other two regions) and strength of song learning in the males that were exposed to the tutor song. There was no such correlation in the other two groups. These results suggest that experience-related neuronal activation is specific to the tutor song and thus unlikely to be a result of differences in attention.

The evolution of intelligence: adaptive specializations versus general process

Darwin argued that between‐species differences in intelligence were differences of degree, not of kind. The contemporary ecological approach to animal cognition argues that animals have evolved species‐specific and problem‐specific processes to solve problems associated with their particular ecological niches: thus different species use different processes, and within a species, different processes are used to tackle problems involving different inputs. This approach contrasts both with Darwins view and with the general process view, according to which the same central processes of learning and memory are used across an extensive range of problems involving very different inputs. We review evidence relevant to the claim that the learning and memory performance of non‐human animals varies according to the nature of the stimuli involved. We first discuss the resource distribution hypothesis, olfactory learning‐set formation, and the ‘biological constraints’ literature, but find no convincing support from these topics for the ecological account of cognition. We then discuss the claim that the performance of birds in spatial tasks of learning and memory is superior in species that depend heavily upon stored food compared to species that either show less dependence upon stored food or do not store food. If it could be shown that storing species enjoy a superiority specifically in spatial (and not non‐spatial) tasks, this would argue that spatial tasks are indeed solved using different processes from those used in non‐spatial tasks. Our review of this literature does not find a consistent superiority of storing over non‐storing birds in spatial tasks, and, in particular, no evidence of enhanced superiority of storing species when the task demands are increased, by, for example, increasing the number of items to be recalled or the duration of the retention period. We discuss also the observation that the hippocampus of storing birds is larger than that of non‐storing birds, and find evidence contrary to the view that hippocampal enlargement is associated with enhanced spatial memory; we are, however, unable to suggest a convincing alternative explanation for hippocampal enlargement. The failure to find solid support for the ecological view supports the view that there are no qualitative differences in cognition between animal species in the processes of learning and memory. We also argue that our review supports our contention that speculation about the phylogenetic development and function of behavioural processes does not provide a solid basis for gaining insight into the nature of those processes. We end by confessing to a belief in one major qualitative difference in cognition in animals: we believe that humans alone are capable of acquiring language, and that it is this capacity that divides our intelligence so sharply from non‐human intelligence.

Imprinting, learning and development: from behaviour to brain and back

Neural and behavioural analyses have shown that the formation of filial preferences in young, precocial birds involves at least two separate processes. One process is an emerging predisposition to approach stimuli with the characteristics of the natural mother. The other (learning) process of filial imprinting results in chicks preferentially-approaching a stimulus to which they have been exposed and involves forming links between the components of the exposed stimulus. The neural substrate for the predisposition is different from that underlying imprinting, and different regions of the chick brain are involved in distinct aspects of learning about imprinting stimuli.

Localized immediate early gene expression related to the strength of song learning in socially reared zebra finches.

Recent evidence showed that exposure of tape‐tutored zebra finch (Taeniopygia guttata castanotis) males to the tutor song involves neuronal activation in brain regions outside the conventional ‘song control pathways’, particularly the caudal part of the neostriatum (NCM) and of the hyperstriatum ventrale (CMHV). Zebra finch males were reared with a live tutor during the sensitive period for song learning. When, as adults, they were re‐exposed to the tutor song, the males showed increased expression of Fos, the protein product of the immediate early gene c‐fos, in the NCM and CMHV, compared with expression in two conventional ‘song control nuclei’, high vocal centre (HVC) and Area X. The strength of the Fos response (which is a reflection of neuronal activation) in the NCM (but not in the other three regions) correlated significantly and positively with the number of song elements that the birds had copied from the tutor song. Thus, socially tutored zebra finch males show localized neural activation in response to tutor song exposure, which correlates with the strength of song learning.

Localized Brain Activation Specific to Auditory Memory in a Female Songbird

Song acquisition in songbird males is a prominent model system for the study of the brain mechanisms of memory. Male zebra finches (Taeniopygia guttata) learn their songs from an adult conspecific tutor early in life. Previous work has shown that exposure of males to their tutor song leads to increased expression of immediate early genes (IEGs) in the caudomedial nidopallium (NCM) and in the caudomedial mesopallium (CMM). In addition, IEG expression in the NCM correlates significantly with the strength of song learning. Interpretation of these findings is complicated, as males both learn the characteristics of tutor song and learn to produce a similar own song. Female zebra finches do not sing, but nevertheless they learn the characteristics of a song to which they were exposed when young, and form a preference for it. Here, adult zebra finch females reared with their fathers showed a significant preference for their fathers song. Females that were later reexposed to their fathers song showed significantly greater expression of Zenk, the protein product of the IEG ZENK, than controls that were exposed to a novel song, in the CMM, but not in the NCM or hippocampus. These results suggest that in female zebra finches the CMM may be (part of) the neural substrate for the representation of the memory of their fathers song. J. Comp. Neurol. 494:784–791, 2006.

How could language have evolved

How could language have evolved? What is the key innovation underlying the evolution of human language? This Essay argues that the ability to “merge” two syntactic elements uniquely explains the recentness and stability of language. [SK to check before publishing on the homepage] CM 16/7

Darwin in mind: new opportunities for evolutionary psychology.

Evolutionary Psychology (EP) views the human mind as organized into many modules, each underpinned by psychological adaptations designed to solve problems faced by our Pleistocene ancestors. We argue that the key tenets of the established EP paradigm require modification in the light of recent findings from a number of disciplines, including human genetics, evolutionary biology, cognitive neuroscience, developmental psychology, and paleoecology. For instance, many human genes have been subject to recent selective sweeps; humans play an active, constructive role in co-directing their own development and evolution; and experimental evidence often favours a general process, rather than a modular account, of cognition. A redefined EP could use the theoretical insights of modern evolutionary biology as a rich source of hypotheses concerning the human mind, and could exploit novel methods from a variety of adjacent research fields.

Causal mechanisms of behavioural development

Introduction Jaap Kruijt G. P. Baerends Part I. Introduction: 1. The concept of cause in the study of behaviour J. A. Hogan 2. Neurobiological analyses of behavioural mechanisms in development J. J. Bolhuis Part II. Development of Perceptual and Motor Mechanisms: 3. The neural basis for the acquisition and production of bird song T. J. DeVoogd 4. Sexual imprinting as a two-stage process H.-J. Bischof 5. The influence of social interactions on the development of song and sexual preference in birds N. S. Clayton 6. Perceptual mechanisms in imprinting and song learning C. ten Cate 7. The development of action patterns K. C. Berridge Part III. Development of Behaviour Systems: 8. The ontogeny of social displays: interplay between motor development, development of motivational systems and social experience T. G. G. Groothuis 9. Psychobiology of the early mother - young relationship A. S. Fleming and E. M. Blass 10. Development of behaviour systems J. A. Hogan Part IV. Development of Cognition: 11. Cortical mechanisms of cognitive development M. H. Johnson 12. Cognitive development in animals D. F. Sherry 13. The biological building blocks of spoken language J. L. Locke Part V. Learning and Development: 14. Behavioural change as a result of experience: toward principles of learning and development P. D. Balsam and R. Silver 15. The varieties of learning in development: toward a common framework S. J. Shettleworth 16. Representation development in associative systems I. P. L. McLaren Index.