James D. Rose

The Neurobehavioral Nature of Fishes and the Question of Awareness and Pain

This review examines the neurobehavioral nature of fishes and addresses the question of whether fishes are capable of experiencing pain and suffering. The detrimental effects of anthropomorphic thinking and the importance of an evolutionary perspective for understanding the neurobehavioral differences between fishes and humans are discussed. The differences in central nervous system structure that underlie basic neurobehavioral differences between fishes and humans are described. The literature on the neural basis of consciousness and of pain is reviewed, showing that: (1) behavioral responses to noxious stimuli are separate from the psychological experience of pain, (2) awareness of pain in humans depends on functions of specific regions of cerebral cortex, and (3) fishes lack these essential brain regions or any functional equivalent, making it untenable that they can experience pain. Because the experience of fear, similar to pain, depends on cerebral cortical structures that are absent from fish brains, it is concluded that awareness of fear is impossible for fishes. Although it is implausible that fishes can experience pain or emotions, they display robust, nonconscious, neuroendocrine, and physiological stress responses to noxious stimuli. Thus, avoidance of potentially injurious stress responses is an important issue in considerations about the welfare of fishes.

Neurophysiological Effects of Vasotocin and Corticosterone on Medullary Neurons: Implications for Hormonal Control of Amphibian Courtship Behavior

Research on a wide variety of vertebrates, from fish to mammals, reveals that corticosteroid hormones and vasotocin-like neuropeptides can potently modulate reproductive behaviors. But, it is not clear how the behavioral effects of these chemical messengers relate to functional properties of behavior-controlling neurons. This problem was investigated in the roughskin newt, Taricha granulosa, an amphibian in which the administration of arginine vasotocin (AVT) facilitates and corticosterone (CORT) inhibits courtship clasping of females by males. In waking, immobilized male newts, neurophysiological effects of AVT and CORT were studied in neurons in the rostral medulla due to the probable role of these neurons in the control of clasping. Topical medullary application of a clasp-facilitating dose of AVT produced a rapid increase in neuronal responsiveness to pressure on the cloaca, a trigger stimulus for clasping responses. Neuronal responses to noncloacal somatic stimuli and to moving visual stimuli were also enhanced. Systemic CORT administration, which has previously been shown to depress newt medullary neuronal sensory responsiveness, reversed the action of AVT such that the peptide depressed sensory responsiveness when applied 30 min after CORT. When AVT application preceded CORT injection by 10-17 min, however, the usual suppressive CORT effect was reversed and this treatment resulted in a rapidly appearing potentiation of neuronal activity and enhanced somatic sensory responsiveness. If the interval between AVT and CORT was increased to 30 min, the steroid caused a rapid depression of firing and a diminished somatic sensory responsiveness in most neurons, similar to what occurs in newts treated with CORT alone.(ABSTRACT TRUNCATED AT 250 WORDS)

Behavioral neuroendocrinology of vasotocin and vasopressin and the sensorimotor processing hypothesis

Vasotocin (AVT) and vasopressin (AVP) are potent modulators of social behaviors in diverse species of vertebrates. This review addresses questions about how and where AVT and AVP act to modulate social behaviors, focusing on research with an amphibian model (Taricha granulosa). In general, the behaviorally important AVT and AVP neurons occur in the forebrain and project to sites throughout the brain. Social behaviors are modulated by AVT and AVP acting at multiple sites in the brain and at multiple levels in the behavioral sequence. This review proposes that AVT and AVP can act on sensory pathways to modulate the responsiveness of neurons to behaviorally relevant sensory stimuli and also can act on motor pathways in the brainstem and spinal cord to modulate the neuronal output to behavior-specific pattern generators. This neurobehavioral model, in which AVT and AVP are thought to modulate social behaviors by affecting sensorimotor processing, warrants further research.

Rapid Neurophysiological Effects of Corticosterone on Medullary Neurons: Relationship to Stress-Induced Suppression of Courtship Clasping in an Amphibian

Courtship clasping of females by male roughskin newts (Taricha granulosa) is rapidly blocked by exposure to corticosterone (CORT). This behavioral effect appears to result from CORT binding to a receptor in neuronal membranes. The present study investigated effects of intraperitoneal CORT administration on neurophysiological properties of extracellularly recorded single medullary neurons in acutely prepared newts. CORT produced multiple neurophysiological effects that emerged within 3 min of injection and increased in magnitude during the next 20-30 min. Spontaneously active and sensory-responsive neurons showed a decline or cessation of firing concomitant with a loss of sensory responsiveness, especially to cloacal pressure, a clasp-facilitating stimulus in behaving newts. After CORT administration, reticulospinal neurons that were backfired (antidromically activated) by spinal cord stimulation, exhibited reduced antidromic action potential amplitude, slowed rates of spike generation and other indications of reduced excitability. Comparable effects of CORT were also evident in newts with a premedullary brainstem transection, indicating a direct hormone action on the caudal neuraxis. Dexamethasone (DEX), a glucocorticoid that binds poorly to the CORT membrane receptor and has little effect on clasping, had little or no direct neurophysiological effect, but DEX injection 30 min before CORT interfered with the neurophysiological action of CORT. The rapidity, time course and specificity to CORT of these neurophysiological effects are consistent with mediation through the CORT membrane receptor. In addition, the pattern and dose sensitivity of these neurophysiological actions plus their occurrence in the medulla, suggest that they could underlie the CORT effect on courtship clasping.

Levels of plasma corticosterone and testosterone in male copperheads (Agkistrodon contortrix) following staged fights.

Fighting behavior between male copperheads (Agkistrodon contortrix) occurs during the two mating periods (late summer/fall and spring) to gain priority of access to females. Fights are characterized by prominent vertical challenge displays, swaying, and a high degree of physical contact that does not involve biting. At the moment of subordination, losers retreat quickly from fights and winners respond by chasing. Subsequently, losers do not participate in further challenge displays or fighting for at least 7 days, and also they show behavioral signs of stress, which includes submissive acts and suppression of sexual behavior. The goal of this study was to determine whether or not losers show elevated levels of plasma corticosterone (B) and depressed levels of plasma testosterone (T) relative to winners and controls. Winners and losers were produced in 13 staged trials. Two different controls (N = 26) were run. Males with no recent agonistic experience were (1) tested in the fighting arena in the absence of a competitive male but paired with a single female (N = 13), and (2) tested alone in their cages (N = 13). All trials, including controls, were conducted in spring and late summer. Mean B in losers at 1-hr postfight was significantly greater than in winners and both control groups in both seasons. Mean T was significantly greater in late summer in all groups, as expected, but in each season was not significantly different between the groups. Levels of B and T were not correlated with SVL, mass, or duration of fighting. This study provides further support for the social insensitivity/challenge hypotheses and is the first to document postfight B and T levels in snakes.

Motor Skills of Typically Developing Adolescents

To identify sex differences and developmental trends in motor performance and coordination across three stages of development: prepubertal, pubertal and postpubertal, 60 participants, 30 males and 30 females, were assessed on 13 motor tasks. Physical characteristics that accompany puberty were used to classify the participants into the stages. Analysis of variance and covariate analyses demonstrated that motor performance improves throughout adolescence in both males and females and that sex differences exist in motor performance, males performing better than females. The magnitude of the stage and sex differences were demonstrated by large effect sizes (?2). The motor tasks of long jump, running speed, and throwing a ball principally distinguished between the males and females. Female performance differed less from male performance after puberty. Results showed no evidence of impaired coordination or awkwardness at puberty for either sex. Implications for rehabilitation specialists include creating awareness to possible sex differences when evaluating childrens motor skills and awareness for the need for further study of motor performance during puberty in children with disabilities.

Corticotropin-Releasing Factor Enhances Locomotion and Medullary Neuronal Firing in an Amphibian

Corticotropin-releasing factor (CRF) administration has been shown to act centrally to enhance locomotion in rats and amphibians. In the present study we used an amphibian, the roughskin newt (Taricha granulosa), to characterize changes in medullary neuronal activity associated with CRF-induced walking and swimming in animals chronically implanted with fine-wire microelectrodes. Neuronal activity was recorded from the raphe and adjacent reticular region of the rostral medulla. Under baseline conditions most of the recorded neurons showed low to moderate amounts of neuronal activity during periods of immobility and pronounced increases in firing that were time-locked with episodes of walking. These neurons sometimes showed further increases in discharge during swimming. Injections of CRF but not saline into the lateral ventricle produced a rapidly appearing increase in walking and pronounced changes (mostly increases) in firing rates of the medullary neurons. CRF produced diverse changes in patterns of firing in different neurons, but for these neurons as a group, the effects of CRF showed a close temporal association with the onset and expression of the peptides effect on locomotion. In neurons that were active exclusively during movement prior to CRF treatment, the post-CRF increase in firing was evident during episodes of walking; in other neurons that also were spontaneously active during immobility prior to CRF infusion, post-CRF activity changes were evident during immobility as well as during episodes of locomotion. Thus, a principal effect of CRF was to potentiate the level of neuronal firing in a population of medullary neurons with locomotor-related properties. Due to the route of administration CRF may have acted on multiple central nervous system sites to enhance locomotion, but the results are consistent with neurophysiological effects involving medullary locomotion-regulating neurons.

Removal of the Vomeronasal Organ Impairs Lordosis in Female Hamsters: Effect Is Reversed by Luteinising Hormone-Releasing Hormone

In female golden hamsters, vomeronasal organ removal disrupts the elicitation of lordosis by lumbosacral tactile stimulation. A similar disruption occurs if the nasopalatine ducts are closed, without removing the vomeronasal organ. Injection of luteinising hormone-releasing hormone reverses the effect of vomeronasal organ removal. These findings suggest that chemosensory signals from the male hamster act via the accessory olfactory system, to facilitate the triggering of lordosis by somatic stimulation.

Disruption of lordosis by dorsal midbrain lesions in the golden hamster

Bilateral lesions of the dorsal midbrain at levels from the anterior to posterior deep tectum abolished lordosis responses to males or manual stimuli. The lesions also blocked reflexive head turning and biting responses to tactile stimulation of the face. Unilateral dorsal midbrain lesions impaired responses to stimuli impinging upon the contralateral body and/or face without affecting lordosis responses to ipsilaterally-applied manual stimuli. The pattern of deficits following unilateral lesions was consistent with the known somatosensory organization of the dorsal midbrain, but the uniform effectiveness of the bilateral lesions placed at any anterior-posterior level of the dorsal midbrain may have been due to bilateral interruption of central gray efferents in addition to deep tectal neuronal damage. Neither bilateral nor unilateral lesions had to involve the central gray to produce their effects.

Rapid, corticosterone-induced disruption of medullary sensorimotor integration related to suppression of amplectic clasping in behaving roughskin newts (Taricha granulosa).

Endogenously secreted or injected corticosterone (CORT) rapidly suppresses courtship clasping in male roughskin newts (Taricha granulosa) by an action on a specific neuronal membrane receptor. Previous studies, using immobilized newts, showed that CORT administration rapidly depresses excitability of reticulospinal neurons and attenuates medullary neuronal responsiveness to clasp-triggering sensory stimuli. The present study used freely moving newts to examine clasping responses and concurrently record sensorimotor properties of 67 antidromically identified reticulospinal and other medullary reticular neurons before and after CORT injection. Before CORT, reticulospinal neurons fired in close association with onset and offset of clasps elicited by cloacal pressure. Reticulospinal neurons also showed firing correlates of nonclasping motor events, especially locomotion. Neuronal activity was typically reduced during clasping and elevated during locomotion. Medullary neurons that were not antidromically invaded (unidentified neurons) usually showed sensorimotor properties that resembled those of reticulospinal neurons. Intraperitoneal CORT (but not vehicle) reduced the probability and quality of hindlimb clasping in response to cloacal pressure, especially within 5-25 min of injection. Simultaneously, responses of reticulospinal and unidentified neurons to cloacal pressure and occurrence of clasping-related activity were attenuated or eliminated. CORT effects were relatively selective, altering clasping-related neuronal activity more strongly than activity associated with nonclasping motor events. The properties of CORT effects indicate that the hormone impairs clasping by depressing processing of clasp-triggering afferent activity and by disrupting the medullary control of clasping normally mediated by reticulospinal neurons. The rapid onset of these CORT effects implicates a neuronal membrane receptor rather than genomic action of the steroid.