Abstract: We ask what cerebellum and basal ganglia “do,” arguing that cerebellum tunes motor schemas and their coordination. We argue for a synthesis of models addressing the real-time role and error signaling roles of climbing fibers. “Synthetic PET” bridges between regional and neurophysiological studies, while “synaptic eligibility” relates the neurochemistry of learning to neural and behavioral levels, [CRÉPEL et al.; HOUK et al.; KANO; LINDEN; SIMPSON et al.; SMITH; THACH; VINCENT]

1. Does the cerebellum control muscles or tune motor schemas? SMITH (sect. 2.2, para. 5) tells us that the mutant mouse Lurcher, in which no Purkinje cells survive beyond early adulthood, “show deficits in both the ability to simultaneously (e.g., asynergia) and sequentially (e.g., dysdiadocokinesia) command the desired muscle synergies.” However, the spinal cat can walk on a treadmill if properly supported and stimulated, and so I would argue that cerebellum serves to adjust the spinal motor schema for walking rather than “commanding” the muscle synergies (For clarity, I will reserve “synergy” for this sense of “muscle synergy,” and “motor schema” for a task-specific “program” of coordinated motor control.) Earlier, SMITH notes “The locomotion was very ataxic and the frequent interruptions from a loss of equilibrium accounted for the absence of modulation in the contralateral limb”; moreover (Smith, personal communication), Lurcher mice can coordinate their limbs for swimming.

Abstract: Cerebellar long-term depression (LTD) is a form of synaptic plasticity, first described by Ito and co-workers, in which simultaneous activation of two excitatory inputs to a Purkinje neuron, parallel fibers (PFs) and climbing fibers (CFs), results in a sustained depression of PF synaptic drive. The purpose of this target article is not to assess the possible role of this synaptic alteration in motor learning, an issue which is addressed by other authors in this volume, nor is it to provide a detailed summary of the work on cerebellar LTD to this point (see Linden & Connor 1993; Crépel et al. 1993 for review) or to place cerebellar LTD within the context of other forms of persistent synaptic depression that occur within the mammalian brain (see Linden 1994b). Rather, it is to discuss results obtained using a very reduced preparation for the study of LTD, embryonic Purkinje neurons grown in culture and stimulated with exogenous excitatory amino acids, and to consider some advantages and limitations of this approach. Recent work using this preparation has suggested that three processes are necessary for the induction of cerebellar LTD: Ca influx through voltage-gated channels, Na influx through AMPA receptor-associated channels or voltage-gated Na channels, and protein kinase C activation – which is dependent upon activation of the metabotropic glutamate receptor mGluR1. In addition, input-specific induction of LTD has been demonstrated in this preparation under conditions where both spontaneous and evoked neurotransmitter release are reduced or eliminated, indicating that postsynaptic alterations are sufficient to confer this important computational property.

Abstract: Long-term depression (LTD) of synaptic transmission at parallel fibre–Purkinje cell synapses is thought to be a cellular substrate of motor learning in the cerebellum. This use-dependent change in synaptic efficacy is induced by conjunctive stimulation of parallel fibres and climbing fibres. Researchers agree that the induction of LTD requires, as an initial step, a calcium influx via voltagegated Ca2+ channels into a Purkinje cell, together with activation of ionotropic (AMPA) and probably metabotropic subtypes of glutamate receptors of this cell. Indeed, due to the lack of specific antagonist, the final demonstration of the contribution of metabotropic receptors in the LTD induction process, under functional conditions, remains unanswered. The debate is now focused on the second-messenger processes leading to LTD of synaptic transmission at parallel fibre-Purkinje cell synapses, after the calcium influx into the cell. All researchers agree that a calcium-dependent cascade of events including activation of protein kinase C is necessary for LTD induction. In contrast, the recruitment in the LTD induction of another cascade, also triggered by Ca2+, that is, through synthesis of nitric oxide and cyclic GMP, remains controversial. On the other hand, growing evidence suggests that these chains of reaction underlying LTD might ultimately lead to a genuine change in the functional characteristics of AMPA receptors at the parallel fibre-Purkinje cell synapses.

Keywords: cerebellum; cGMP; desensitization; excitatory amino-acid receptors; nitric oxide; protein kinase C; synaptic-plasticity.

THE COGNITIVE TURN IN PSYCHOLOGY

We have seen that an adequate scientific account of moral agency must include reference to our cognitive capacities. The questions of how we acquire and put into action our moral capacities cannot be answered satisfactorily by appealing only to evolutionarily based and learned, but noncognitive, moral capacities. In particular, we saw in Chapter 5 that the Skinnerian claim that the science of operant behavior is the science of values fails because it does not take account of the cognitive features of human agency. Our conclusion rested in large part on the findings of psychologists who have shown that cognitive factors play a role in the explanation of human behavior. This turn to the cognitive in psychology is not reserved for critics of behaviorist theory; it is part of what has come to be called the cognitive revolution in psychology, which has taken two forms. For want of better descriptions, I shall call one cognitive revolution the representational revolution and the other the agential revolution. The representational revolution focuses on human knowledge-gaining capacities and achievements. It has developed in the areas of perception, memory, imagery, language, thought, and problem solving. The agential revolution is concerned with issues of human action. It has emerged in the areas of learning, motivation, personality, social psychology, and abnormal psychology.

MORAL AGENCY

We begin by considering an ordinary perspective on being a moral agent. By an ordinary perspective I mean one that is shaped by our ordinary experience of and reflection on being a moral agent. You can probably recall many small and some very large moral decisions in your life. Some of these are more personal — regarding, for instance, telling the truth in a situation where the truth was rightfully demanded, but it was in your interest to be silent or to shade your story. Some decisions may have been more communal — whether, for instance, your professional group or union should actively oppose or support the right of a woman to have an abortion. Many decisions, no doubt, concerned issues in which science and technology played some part in both the problem and possible solutions. Should I carpool? Should I support a movement in Congress to eliminate funding for environmental protection? What does the ordinary perspective on moral agency say about moral agency given experiences of the preceding sort and reflection on them? It probably says a lot of different things since, on one level, there are as many experiences and reflections as experiencers and persons reflecting on their experiences. However, let's generalize and see if we can say some broad things about moral agency.

Abstract: Brindley proposed that we initially generate movements “consciously,” under higher cerebral control. As the movement is practiced, the cerebellum learns to link within itself the context in which the movement is made to the lower level movement generators. Marr and Albus proposed that the linkage is established by a special input from the inferior olive, which plays upon an input-output element within the cerebellum during the period of the learning. When the linkage is complete, the occurrence of the context (represented by a certain input to the cerebellum) will trigger (through the cerebellum) the appropriate motor response. The “learned” movement is distinguished from the “unlearned” conscious movement by its now being automatic, rapid, and stereotyped. The idea is still controversial, but has been supported by a variety of animal studies and, as reviewed here, is consistent with the results of a number of human PET and ablation studies. I have added to the idea of context-response linkage what I think is another important variable: novel combinations of downstream elements. With regard to the motor system and the muscles, this could explain how varied combinations of muscles may become active in precise time-amplitude specifications so as to produce coordinated movements appropriate to specific contexts. In this target article, I have further extended this idea to the premotor parts of the brain and their role in cognition.

Having solved the investigative dilemma facing scientific students of moral agency, thereby avoiding an ill-fated choice between a scientifically adequate but morally irrelevant account of agency and a morally relevant but scientifically inadequate account of agency, I concluded the previous chapter on a note of cautious optimism. The solution came by showing that a four-level model of moral agency based on Bandura's social cognitive theory of agency not only provides empirically well-grounded answers to major questions about how humans acquire and put into action their capacities as agents, but also more than meets the criteria for what counts as moral agency. However, my optimism is necessarily tempered by the realization that the investigative dilemma is only part of a larger challenge, what I call the reductionist predicament, facing any scientific naturalistic account of moral agency that takes as its goal to do justice both to the phenomenon of moral agency and to the scientifically established facts of agency. Reductionists and eliminativists are suspicious of the scientific adequacy of the psychological theories that I have invoked in the solution of the investigative dilemma. They question the scientific adequacy of theories that are formulated in terms of intentionalistic categories, whether of the folk psychological or of the information processing sort, or some combination thereof.

Do we actually have evolutionarily based moral capacities? Three prominent contemporary biologists, among others, have addressed that question in some detail and given it significantly different answers. Although all three have taken broadly interactionist stances, after that they part ways. George C. Williams (1988a,b, 1989) has adopted an antagonistic interactionist stance, arguing that biology and morality are in mortal combat with each other. For Williams, the ends of evolutionary processes, whether the ultimate ones of survival and reproduction or the proximate ones of various adaptations, are morally tainted and conflict with morality. Richard Alexander (1979, 1985, 1987) puts morality in the service of biology, viewing evolutionary ends as morally neutral. E. O. Wilson (1978) places biology in the service of morality, and argues that they provide the bases for morality. I shall examine both Wilson's proposal and the support that he brings for it and argue that Wilson's evolutionary story about morality cannot be the full story. Although the support that he offers for the existence of evolutionarily based moral capacities is suggestive, much more evidence is needed to make his plausible suggestion into a well-supported hypothesis. In the following chapter, I attempt both to expand Wilson's evolutionary story and to argue for an integrationist approach by shifting our focus to development and the ontogeny of moral capacities.

INTRODUCTION

In 1974, Ernst Mayr published a now classic paper on the distinction between innate and acquired characteristics. In this work, Mayr broke away from some of the more confining features of traditional accounts of innateness, and proposed a dimension along which behaviors might be expected to vary with respect to innateness. Mayr proposed a distinction between “closed” and “open” programs1 – a program that does not allow appreciable modifications during the lifespan of its owner is a “closed” program, while a program that does allow for the effects of additional input is “open.” Since it seems unlikely that any developmental program can be completely closed, Wimsatt (1986) has suggested that Mayr's notion of a closed program may be most fruitfully viewed as a relative one – “relative to the period of time of development under investigation, and the class of inputs being investigated, and probably also to the environment and the prior state of the developing phenotype” (Wimsatt 1986, p. 203). In Wimsatt's terms, a closed developmental program is one which is canalized with respect to the relevant inputs.

Mayr's classificatory schemes distinguished two types of behavior: A behavior is considered communicative if it is directed toward a recipient who is capable of responding with behavior of its own, and noncommunicative if it is directed toward a “recipient” that is passive and does not itself react (e.g., behaviors involved in selecting a habitat or seeking food).

INTRODUCTION

Striking parallels exist between the development of speech in human infants and the development of song in birds. Many sparrows, for example, learn their songs more readily during a sensitive period than at other times during development, require practice, and must hear themselves sing for normal song to develop (Baptista & Petrinovich 1986). These same features characterize both the earliest speech of human infants (see e.g., Ferguson et al. 1992) and second language learning, whether spoken or signed, among older individuals (Johnson & Newport 1989). Song production in zebra finches and canaries, like speech production in humans, is under lateralized neural control (Arnold & Bottjer 1985; Nottebohm 1991). Damage to any one of these areas, like damage to Broca's or Wernicke's area in (usually) the left temporal cortex of the human brain (for reviews, see Caplan 1987, 1992), produces highly specific deficits in the production or processing of communicative sounds.

As a result of these parallels in both behavior and neurobiology, studies of avian song development currently provide the best animal model for research on the mechanisms underlying speech development (Marler 1987). In contrast, while nonhuman primates are our closest living relatives and have often been used as animal models for the study of human social development (see e.g., Hinde 1984), their vocal communication is generally thought to provide no useful parallels with the development of human speech.

INTRODUCTION

In this chapter, we review work on the nature of vocal learning in human primates, comparing them en passant to nonhuman primates who share many of their capacities but are both less eager and less successful vocal learners. The basic question underlying this review is whether the precocious and prolific vocal learning of human primates can be explained by biological mechanisms that are specific to the language system or whether it relates to more general social capacities and to the particular social context of vocal learning in humans.

We know that young human primates are particularly good at vocal learning. One bit of evidence in support of this contention is that all national languages are spoken, even though extremely subtle articulatory and auditory discriminations are relied on to carry meaning in spoken languages. In addition, babbling and vocal play are early developmental activities universally observed in normally developing children (Locke 1992; Locke & Pearson 1992). Imitative vocal behavior is also universal in young children and common even in more mature language users. Furthermore, language learning, particularly word learning, by young children, is quite rapid and efficient.

Although there is much emphasis on children's preparedness for language learning, in fact children everywhere seem to enter the language system of conventional words use through the use of vocal forms that are more like adult forms in sound than in semantic or syntactic function. These early forms could be argued, though, to foreshadow a major function of oral language even in adulthood, namely to effect participation in social interaction rather than transmission of information.

INTRODUCTION

Vocal learning in birds has evolved independently in several different avian orders, but is common in only two groups, oscine songbirds and parrots. The diversity and complexity of vocal repertoire structure among the species in these two groups is enormous. However, much scientific attention in avian song learning has focused on a small group of songbirds, north temperate migrant species, in which song is restricted mainly to males and the occurrence of song and territoriality is seasonal. In addition to these birds there is also a vast number of laboratory studies on the development and neural control of male song in the zebra finch (Taenopygia guttata), an Australian species with an unusually compressed developmental period. This large body of research has resulted in general models of song and vocal learning drawn from only a small subset of the world's birds.

While these many studies have broadened our understanding of learned vocal communication, it is our contention that there is much to be gained by study of the vocal behavior of avian species with more complex social relationships. Such species exhibit long-term associations between well-acquainted individuals, and, for many, longterm associations are related to permanent residence in an area. Another important characteristic is the tendency to live in stable groups for at least part of the year. These groups could be, for example, a winter foraging flock of chickadees, a breeding colony of caciques, a foraging flock of cockatoos, or a permanently territorial pair of tropical wrens.

By consideration of common features of disparate groups that represent more fully the portion of the world's birds that learn vocally, we can approach a more truly universal model of vocal learning.

INTRODUCTION

Most studies of the effects of social interaction on the ontogeny of vocal communication in birds and primates concentrate on the normal course of development of species-specific codes: how birds learn conspecific song, how nonhuman primates develop their natural repertoire of calls, and how human infants develop language. The effects of social interaction, however, are probably even more important during exceptional learning (Pepperberg 1985): learning that is unlikely to occur in the normal course of events. Such learning, defined and described below, has been documented for a number of species, including humans. I have been particularly interested in examining how social interaction can influence a specific type of exceptional learning – the development of interspecies communication between humans and birds. My research on the effects of social interaction on the acquisition of a vocal, English-based code by grey parrots (Psittacus erithacus) clearly demonstrates how social and environmental input1 can engender learning that would not otherwise occur (e.g., Pepperberg 1990a). Interestingly, an analysis of research on ape language also demonstrates how social interaction may be a particularly effective means of teaching nonvocal human-based communication codes to nonhuman primates.

Although characterizing the effects of social and environmental influences on exceptional learning is not a simple task, my work has shown that a conceptual framework, social modelling theory, can be used (a) to characterize how social input influences learning and (b) to delineate the critical features of input necessary for exceptional learning.

INTRODUCTION

Marine mammals stand out among nonhuman mammals in their abilities to modify their vocalizations on the basis of auditory experience. While there is good evidence that terrestrial mammals learn to comprehend and use their calls correctly, there is much less evidence for modification of vocal production (Seyfarth & Cheney, Chapter 13). In contrast, vocal learning has evolved independently in at least two marine mammal taxa, the seals and cetaceans, and is widespread among the whales and dolphins. We concentrate our focus in this chapter on vocal learning and development in the bottlenose dolphin (Tursiops truncatus) because it is the marine mammal species in which vocal learning and imitation has been best studied.

Dolphins produce a variety of sounds. The two predominant sound types are clicks, which can be used for echolocation, and frequency-modulated whistles, which are used for social communication. In addition to whistles, dolphins produce short frequency upsweeps that have been called chirps (Caldwell & Caldwell 1970). The dolphin vocal repertoire also includes a variety of burst pulsed sounds and combinations of pulses and whistles.

Captive bottlenose dolphins of both sexes are highly skilled at imitating synthetic pulsed sounds and whistles (Caldwell & Caldwell 1972; Herman 1980). Once a dolphin learns to copy a sound, the novel sound can be incorporated into its vocal repertoire, and the dolphin can produce the sound even when it does not hear the model. Bottlenose dolphins may imitate sounds spontaneously within a few seconds after the first exposure (Herman 1980), or after only a few exposures (Reiss & McCowan 1993).

INTRODUCTION

Songbirds learn their songs by hearing others and then copying them, matching or improvising on the song theme (Slater 1989; Catchpole & Slater 1995). Their social behavior varies among species – they are migratory or resident, solitary or group-living, faithful partners to a single mate, polygynous or with no pair bond, and parental or nonparental in the care of their offspring (brood parasites lay in nests of other species, and their fosterers rear the young). All songbirds depend on parental care, and it has been suggested that this is the time when the young learn their songs. Later, when they are independent, the birds engage in a wider range of social interactions.

Field studies suggest that most songbirds learn their songs after the time of natal dispersal, when a bird moves from the site where it was reared to an area where it copies the song of a neighbor, rather than singing the song of its father: Bewick's wrens (Thryomanes bemickii), marsh wrens (Cistothorus palustris), saddlebacks (Philesturnus carunculatus), indigo buntings (Passerina cyanea), white-crowned sparrows (Zonotrichia leucophrys), and corn buntings (Emberiza calandra) (Kroodsma 1974; Verner 1976; Jenkins 1978; Payne et al. 1987; Baptista & Morton 1988; Petrinovich 1988; McGregor & Thompson 1988; McGregor et al. 1988). Song sparrows (Melospiza melodia) copy at least one song from three or four neighboring males when they settle on a territory, some time after the first four weeks of life (Nice 1943; Beecher et al. 1994). In two species males often copy their father (Darwin's finches (Geospiza fortis), zebra finches (Taeniopygia guttata); Millington & Price 1985; Gibbs 1990; Zann 1990), but not all individuals do this.