John C. Fentress

Interrupted ongoing behaviour in two species of vole (Microtus agrestis and Clethrionomys britannicus). I. Response as a function of preceding activity and the context of an apparently ‘irrelevant’ motor pattern

Abstract Microtus agrestis and Clethrionomys britannicus were maintained under different home pen conditions and tested in a large alley. Ongoing behavioural sequences were continuously recorded and interrupted at set intervals by an overhead moving object. Two main problems were examined. First, does an animals response to the experimental stimulus vary as a consequence of different ongoing behaviour? Secondly can systematic increases as well as decreases in a seemingly irrelevant (i.e. ‘displacement’) behaviour be observed? Consequences of the differences in temperament between the two species, of the different home pen conditions, and of different intensities of the experimental disturbance were also explored. When locomotor activity preceded the stimulus presentation, fleeing rather than just freezing was most likely to occur. The role of an underlying ‘activity tendency’ which need not be expressed in overt locomotion was suggested by the fact that the more docile Microtus was generally more active in the experimental alley, and also fled more than Clethrionomys even when the two species were matched for behaviours preceding the stimulus. This hypothesis was supported by the subsequent finding that locomotor behaviour which had ceased several seconds before the stimulus presentation also increased flight probability. Home pen cover plus trial number influenced flight probability and appeared to combine in their effect with one another and with ongoing locomotion. Other ongoing activities such as grooming appeared on occasion to be momentarily accelerated by the stimulus presentation, but were soon suppressed. Microtus groomed more after the stimulus presentation than during control trials. Clethrionomys groomed less. Microtus also groomed more and Clethrionomys less following a high intensity compared with a low intensity disturbance. These data suggested that the animals were most likely to groom when optimally ‘aroused’. A temporal analysis of grooming supported the basic model. A single unitary process, however, could not be assumed. The ‘disinhibition hypothesis’ was partly supported by the data for grooming, but possible limitations were noted. For example, the relation between grooming and subsequent locomotion was inconsistent. An increase in the apparent intensity of grooming after the stimulus presentation was occasionally observed. Home pen cover had minimal effect upon grooming, probably as a consequence of housing numerous animals together. The relevance of these findings to problems of behavioural integration, and most particularly to the issue of specific versus general motivational systems, is discussed.

Specific and Nonspecific Factors in the Causation of Behavior

In dealing with patterned behavior, an immediate question concerns the degree to which different component activities are separate from one another in their control. Models of integrative specificity stress separate control mechanisms for different behavioral components. Nonspecific models stress mechanisms that are shared among many different activities. Each of these models has certain merits but also certain limitations. Section II of this paper provides a brief outline of some of the major aspects of both the action-specific models and the diffuse activation models of integrated behavioral control. It is suggested that much of the apparent controversy is due to inconsistent application of classificatory criteria which are often not adequately defined. For the purpose of illustration, these issues are discussed in terms of the ethological construct of “action-specific” control and the neuropsychological dimension of “nonspecific” activation. A possible alternative position that stresses overlapping control systems and partial specificity is introduced. Section III concerns aspects of classification and analysis plus some related conceptual issues that appear most relevant to current thoughts about specific vs. nonspecific behavioral control. It is pointed out that themost strict criterion for specific control is a system that involves only a single input and a single output and that is entirely independent in its operation from other activities in other control systems, while the most strict definition of nonspecific control is that all inputs affect all outputs, identically. Neither of these criteria is likely to be met, and a more limited operational approach is suggested. It is particularly clear that the problem of input specificity is partially separable from that of output specificity, and that “nonspecific” models at one level of analysis may reflect the operation of “multispecific” mechanisms at a different level of analysis. It is emphasized that input/output analyses provide a logic for the interpretation of intervening processes and do not permit simple S-R models. Section IV provides a detailed literature review that illustrates these and related issues. The data indicate a need to consider separately, and then synthesize, the operation of (1) qualitative variables (which inputs and which outputs), (2) quantitative variables (how much of these inputs and/or outputs), and (3) temporal variables (which part of the input/output sequence). The possible importance of encoding mechanisms (e.g., habit strength) is also briefly considered. Section V reviews the ethological literature on displacement activities as a particularly clear illustration of major issues in specific vs. nonspecific control. It is demonstrated that recent emphasis upon (1) disinhibition as a result of behavioral competition and (2) the operation of specific exogenous and peripheral stimuli provides a useful supplement to models of “nonspecific” endogenous activation. However, it is also suggested that endogenous excitatory processes may be partially shared among competing behavior patterns under certain circumstances and in that sense be “nonspecific.” Section VI provides a synopsis of the major issues discussed previously and outlines a “boundary-state” approach that appears to avoid many of the difficulties of strict specific and nonspecific models. This approach stresses both partial and shifting overlap among control systems as a function of intensity and temporal parameters. An analogy is suggested to the center/surround organization of control systems at the neurological level. Integrative pathways are viewed to become more or less focused as a function of the balance between excitatory and inhibitory mechanisms. This balance between excitation and inhibition may shift in a systematic manner as a joint function of qualitative, quantitative, and temporal dimensions employed in a given analysis.

Interrupted ongoing behaviour in two species of vole (Microtus agrestis and Clethrionomys britannicus). II. Extended analysis of motivational variables underlying fleeing and grooming behaviour

Abstract Experiments were designed to examine two previously proposed variables: (a) an ‘activity tendency’ which results in increased probability of fleeing; (b) an ‘optimal arousal’ range in which grooming is most likely to occur. Wild-trapped Microtus agrestis and Clethrionomys britannicus were individually housed and tested in the previously employed experimental alley. The probability of fleeing behaviour was greatly increased when overt locomotion was either concurrent with or ceased within 10 sec of the experimental disturbance. The concept of a temporarily persisting ‘activity tendency’ which in itself affects fleeing was supported. Amphetamine increased fleeing and Nembutal decreased fleeing to an extent that could not be accounted for solely in terms of current or recently ceased locomotion. Differences between species and cover conditions were equivocal, perhaps due to the high tendency of individually housed animals to flee. Two main techniques for studying the previously defined ‘optimal arousal’ model for grooming were (1) to examine integration of home pen cover plus amphetamine and Nembutal with species differences in grooming, (2) attempt to manipulate ‘arousal’ over a wide range with the two drugs. Cover and 0·8 mg per kg amphetamine produced more grooming in Microtus while no cover and 15 mg per kg Nembutal produced more grooming in Clethrionomys, as predicted from the ‘arousal’ model. Further, the drug and cover inputs combined in their effect. Each species showed an overall non-linear relationship between drug dose and grooming as expected from the model. Certain inconsistencies with the model were also noted in the present experiments, however, and the possibility that both ‘arousal’ and ‘conflict’ models are necessary is discussed. The increase in grooming intensity was again noted, particularly under amphetamine, as was the increased probability and vigour of other simple motor patterns with this drug. Problems of integration of multiple inputs with patterned outputs are discussed further.

The Development of Action Sequences

Many years ago, [Lashley (1951)] challenged behavioral neuroscientists to examine movement properties and the serial order of behavior more specifically. This was in many respects a logical follow-up of [Hebb’s (1949)] concerns with the organization of behavior, according to which, individual behavioral and brain properties must be isolated, but also examined within broader contexts of expression ([Fentress, 1999]). For example, Hebb devised concepts of cell assembly and phase sequence to help behavioral neuroscientists evaluate the fact that all behavior is organized in time. Movement is a directly observable manifestation of this dynamic ordering in brain and behavior ([Berridge & Whishaw, 1992]; [Fentress, 1990], [1992]; [Golani, 1992]; [Kelso, 1997]; [Thelen & Smith, 1994]). As such, quantitative analyses of movement can provide fundamental insights into brain—behavior organization, including the developmental profiles that occur dynamically across levels and time frames of operation. As stated by [Churchland and Sejnowski (1992], p. 178), “Our brains are dynamical, not incidentally or in passing, but essentially, inevitably, and to their very core.” As will become clear in this chapter, we agree with this position, and believe that action dynamics can provide fundamental insights into processes at both onto-genetic and integrative time frames of organization

Revisiting the concept of behavior patterns in animal behavior with an example from food-caching sequences in Wolves (Canis lupus), Coyotes (Canis latrans), and Red Foxes (Vulpes vulpes)☆

We discuss the history, conceptualization, and relevance of behavior patterns in modern ethology by explaining the evolution of the concepts of fixed action patterns and modal action patterns. We present the movement toward a more flexible concept of natural action sequences with significant degrees of (production and expressive) freedom. An example is presented with the food caching behavior of three Canidae species: red fox (Vulpes vulpes), coyote (Canis latrans) and gray wolf (Canis lupus). Evolutionary, ecological, and neuroecological/neuroethological arguments are presented to explain the difference in levels of complexity and stereotypy between Canis and Vulpes. This article is part of a Special Issue entitled: Canine Behavior.

Emotional networks: The heart of brain design

The concept of emotion as defined by Rolls is based upon reinforcement mechanisms and their underlying neural networks. He shows how these networks process signals at many levels, through both separate and convergent pathways essential for adaptive action. While many behavioral issues related to emotion are omitted from his review, he succeeds admirably in summarizing both the “current state of the art” in single unit analyses and in pointing out how future research directions may be crafted.