PHYSIOLOGICAL ETHOLOGY OF SOCIAL DOMINANCE

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PHYSIOLOGICAL ETHOLOGY OF SOCIAL DOMINANCE

• NEURAL and ENDOCRINE CAUSES and CONSEQUENCES of
  SOCIAL BEHAVIOR

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Domains of Ethology

• DESCRIBE
• Development
• Ecology
• Evolution
• Physiology
• DEEP ethology

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Background Blue Spiny Lizards

• Ethology
• Physiological Ecology

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Background Green anoles

• Ethology
• Display Behavior
• Social interactions
• Aggression

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Background Neurology

• Describe brain anatomy in detail

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Background Neurology

• Establish atlas of brain structures

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Background Neurobehavior

• Basal forebrain dysfunction causes social
  agnosia for aggression
• Other behavioral patterns unaffected
• Amygdala dysfunction causes social agnosia for
  courtship

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The Anolis Model

• Small, easily maintained,
• displays focal behavioral patterns easily in
  laboratory
• Dermal chromatophore responds only to circulating
  hormones

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Lizard Dominance

• After an initial period of mutual testing for
  strength and stamina
• Dominants remain green and subordinates become
  brown and adopt distinctive postures.

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Establishment of social dominance hierarchy
Behavioral changes

• Color significantly darker in subordinates
• Posture comparable, subordinates slightly lower
• Site selection significantly lower in
  subordinates
• Will NOT court females

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Behavioral endocrinology of Anolis social
dominance

• Aggressive interactions evokes an acute stress
  response in both combatants (eyespot is
  definitive)
• shorter latency to response is much more likely
  to win
• Elevated testosterone shortens latency
• After interaction, winners have higher NE levels
• -Summers Greenberg 1994

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Behavioral neurophysiology of Anolis social
dominance

• Midbrains of dom/sub pairs of male anoles were
  examined at 1 hr, day, week, month after initial
  interaction
• Subs had elevated serotonin (5-HT) activation
  within an hour (5HT also inhibits aggression)
• Subs had reduced adrenergic activation at first
  and then increased with time
• -Summers Greenberg 1995

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Laboratory and Field

• Neural, endocrine, and behavioral dynamics
  becoming progressively more clear in the highly
  abstract context of the lab
• Now to reconcile with what is actually seen in
  the field
• Social subordinates rarely seen

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Chromomotor model for the stress response

• Acute, repetitive, or sustained stressors are
  integrated in the CNS
• Autonomic neurons activate the adrenal medullary
  response
• H-P-A axis integrates the adrenal cortical
  response
• The Anolis body color thus reflects underlying
  neuroendocrine coping activities
• Body color reflects autonomic tone

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MSH and aggression

• Acute stress depletes MSH
• Agonistic winners manifest typical stress
  response down (56 (of control values)
• Agonistic losers, MSH is slightly up (127 (of
  control values)
• Social Dominants, MSH is slightly up (128 of
  control values)
• Social Subordinates, MSH is significantly up
  (217 of control values)

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PUTATIVE INFLUENCES ON MSH RELEASE

• !CRF increases circulating levels (Proulx-Ferland
  et al. 1982)
• !ACh increases circulating levels (see Hadley
  Bagnara 1975)
• !SEROTONIN may be MSH-RF (see Hadley Bagnara
  1975)
• !CATECHOLAMINES (EPI, NOREPI, DOPAMINE) may
  inhibit MSH release from pars intermedia (see
  Hadley Bagnara 1975)
• !ENDORPHIN reduces MSH binding
• !STRESSORS aggression raises pituitary content
  (Francis Peaslee 1974), with increased ACTH)
• ! BEHAVIOR activity decreases MSH in goldfish
  (but not in rats) acute stress (chase or
  restraint) reduces MSH in anoles aggression
  reduces it in winners but increases it in losers
  chronic stress (social subordination) increases
  MSH (Greenberg, Chen, and Vaughan 1986)

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PUTATIVE EFFECTS OF MSH RELEASE

• ! AGGRESSIVENESS is diminished (Patterson et al.
  1980)
• ! "EMOTIONALITY" is decreased (Golus et al. 1979)
• ! TONIC IMMOBILITY, duration decreased (Stratton
  Kastin 1976)
• ! "MOTIVATION" is increased (Stratton Kastin
  1973)
• ! ATTENTION is enhanced (Kastin et al. 1971)
• ! ANXIETY is reduced (Miller et al. 1974)
• ! ACTH release is increased (Lis et al. 1982)
• ! AGGRESSION can be evoked (in mice) by release
  of a pheromone facilitated by MSH synergy with
  testosterone (Nowell et al. 1980)
• ! TROPHIC PROPERTIES indicated by stimulation of
  fetal growth, protein synthesis, wound healing,
  and liver regeneration (see Swaab and Martin 1981)

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Establishment of social dominance hierarchy CS
changes and effect of castration

• I X I, subordinates have elevated CS
• I X C, subordinates not significantly higher
• C X C, subordinates not significantly higher

Anecdote some castrates become a relentless
subordinate, testing the dominant every day.
(Intact losers quit after 3 days.) Eventually
dominants show repetitive stress syndrome.
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IMMEDIATE PHYSIOLOGICAL CONSEQUENCES OF LOSING

• CATECHOLAMINE SURGES (body color, nuchal crest
  erection, Greenberg et al. 1984)
• NE LOWER RELATIVE TO WINNER (Summers Greenberg
  1994)
• CORTICOSTERONE INCREASED (Greenberg et al. 1984)
• MSH INCREASED (relative to winners, Greenberg,
  Chen, and Vaughan 1986)
• SEROTONIN ACTIVITY INCREASED IN THE MIDBRAIN,
  HIND BRAIN (Summers Greenberg 1995),
  HIPPOCAMPUS, AND NUCLEUS ACCUMBENS (Summers et
  al. 1998)

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LONG-TERM PHYSIOLOGICAL CONSEQUENCES OF LOSING

• ANDROGEN REDUCED (Greenberg Crews 1990)
• CORTICOSTERONE ELEVATED (Greenberg et al. 1984)
• MSH INCREASED (relative to dominants, Greenberg,
  Chen, and Vaughan 1986)
• DOPAMINE ACTIVITY DIMINISHED, ADRENERGIC ACTIVITY
  ENHANCED IN THE MID AND HIND BRAIN (but back to
  control values by one month) (Summers Greenberg
  1995)

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EFFECTS of CORTICOSTERONE

• CS-implanted A sagrei reduced approach and
  aggression (Tokarz 1987)
• CS-implanted Uta reduced aggression even if
  implanted with testosterone (DeNardo Licht
  1993)
• CS-implanted A carolinensis initial agonistic
  responses vigorous but rapidly manifest
  submissiveness when adversary answers display
  (Greenberg unpubl pilot study)

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LIFE AS A SUBORDINATE

• Many dominant/subordinate pairs stabilize and can
  maintain long-term relationship
• Subordinates do not typically succumb to
  diseases of adaptation
• Contribution from trophic MSH effects?
• Contribution from androgen reduction?

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EFFECTS of CASTRATION

• Could androgen reduction be stress-adaptive?
• Castrated A. carolinensis in fights, latency
  duration of EPI-dependent eyespot extended
  (Summers Greenberg 1984)
• Castrated A. carolinensis subordinates -body
  color not significantly darker, circulating CS
  not significantly higher than dominants or
  isolates (Greenberg et al. 1984)
• In A. carolinensis, acute stress impairment of
  exploratory responses in a novel habitat much
  less severe in castrates (except for airlicking,
  Greenberg 1993)

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EFFECTS of ANDROGEN IMPLANTS

• Prospective adversaries both had testosterone
  implants
• Social dominance relationship established but
  subordinate androgen levels could not be reduced
• Anticipated continuing stressful exchanges never
  occurred, the subordinate had enhanced attention
  to the dominant and was effectively a
  super-subordinate.
• Unlike typical subordinates, an
  androgen-implanted subordinate would court
  females whenever the dominant was out of sight.

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SURVEY subclinical effects of stress on behavior

• STRESS was defined for the last 75 years in terms
  of its effects on VITAL FUNCTIONS (such as
  homeostasis)
• Chronic or uncontrollable stress leads to
  REALLOCATION of an organisms resources
• As survival priorities are readjusted, DISEASES
  OF ADAPTATION emerge (hypertension,
  gastro-intestinal dysfunction, immuno-suppression)
  
• Levels of stressors often follow a U-shaped
  curve manifesting paradoxical and reversal
  effects

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SUBCLINICAL EFFECTS stress-sensitive behavior

• Detection, Arousal and Attention (steroids affect
  sensory thresholds, EPI intensifies acute CS
  enhances salience)
• Activity (CRF facilitates in familiar habitat,
  inhibits in unfamiliar habitat)
• Exploration (CRF and ACTH enhances effects of
  novelty, CS facilitates)
• Learning and memory ( EPI, CRF, MSH facilitate
  acquisition)
• Cognition ( catecholamine modulation taking
  prefrontal cortex offline (Arnsten))

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SURVEY stress-sensitive behavior

• Feeding ( CS stimulates or inhibits depending on
  circulating levels)
• Aggression (ACTH suppresses, CS increases or
  decreases depending on circulating levels)
• Social Dominance (CS increases submissiveness)
• Reproduction ( ACTH, CS, opiods, and prolactin
  impair HPG axis)
• Dysfunctional behavior (stereotypies, neuroses,
  psychoses)

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Anolis exploratory behavior

• Posture and site-changes, tongue-touches and
  airlicks increase in a new cage IF first mildly
  stressed (handling)
• All exploratory behaviors except air-licking
  suppressed by more intense stress (evoke
  eye-spot)
• Castration ameliorates the suppressive effect of
  intense stress

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Aggression and Dominance in Anolis

• Many lizard species manifest an apparent
  continuum from strict territoriality to social
  dominance hierarchies (Chas Carpenters
  experiences, Hunsaker Burrage 1969)
• Is there a dominance threshold?
• Anolis carolinensis males spontaneously establish
  dominance relationships in laboratory (and in the
  field, smaller hidden males supplant
  conspicuous dominants removed for testing Todd
  Campbell)

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Future use of the Anolis model

• Key observations of basal forebrain function
  relative to aggression and dominance have been
  corroborated by labs researching OCD
  dysfunctional stereotypies (Lew Baxter
  colleagues at UAB Med)
• Forebrain 5-HT incr acutely in doms but
  decreases in subs
• Doms (but not subs) have incr dorsolateral basal
  ganglia activation (2DG experiments)

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Future use of the Anolis model

• A. carolinensis and A sagrei manifest differences
  in brain function that correspond to differences
  in behavior (sensu oxytocin in voles)
• Prospective doms have a higher tonic level of
  activity than do subs
• Doms did more patrolling than subs
• Doms subs spent less time in visual proximity
  than would be expected by chance (Harris
  Greenberg)

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SURVEY Basal Ganglia

• MOTOR FUNCTIONS
• Interface with amygdala which energizes action
• Inhibition of competing motor functions
• SENSORY FUNCTIONS
• Somatosensory and visual discrtimination
• COGNITIVE FUNCTIONS
• Sequence planning
• Expectations
• Attention
• creativity (activation buy reafferent cognitive
  dissonance and positive affect of teathered
  novelty)

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STRESS and the EVOLUTION of BEHAVIOR

• The Ritualization of signals a model
• fragments of motor patterns or autonomic
  reflexes become temporally or spatially
  associated as an ensemble (Morris 1956, Hinde and
  Tinbergen 1958)
• The Central Adaptation Syndrome (Huether 1996).
• Controllable stressors lead to a go and
  specialize strategy (e.g., earlier recognition
  and avoidance, improved fighting strategies,
  refined submission behavior)
• Uncontrollable stressors lead to a wait and
  reorganize strategy (e.g., CS reorganization of
  neural circuits tuning of learning, motivation,
  and emotional states)

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STRESS and the EVOLUTION of BEHAVIOR

• Stress-sensitive intersections of motivation,
  affect, and cognition are candidates for
  evolutionary change.
• Valence of affect positive, cortical-limbic
  areas negative, subcortical-limbic areas
  (Paradiso et al. 1999)
• note male anoles with subcortical lesions act
  like castrates- they attend stimuli but
  appear unmotivated to respond aggressively
  (social agnosia, recalling autistic failure
  to recognize signals)
• Active versus passive coping parallel autonomic
  strategies correlated with activity in discrete
  columns of periaquaductal gray (Bandler et al.
  2000)

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STRESS and the EVOLUTION of BEHAVIOR

• Conclusion
• The dynamics of the stress response has
• (a) multiple individual elements (which may be
  pleiotropic) and
• (b) specific alternate pathways from afference,
  through the brain, thence to efference.
• Many of these can be selectively emphasized or
  diminished and put in the service of other
  functions through the process of bricolage
  comparable to the ritualization of social
  signals.
• Pathways selected can influence
• (a) apparent controllability of input
• (b) affect (positive or negative)
• (c) coping (active versus passive)

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STRESS and the EVOLUTION of BEHAVIOR

• NEW DIRECTIONS
• Data on the neuro-modulating effects of stress
• on specific brain sites suggests how
  behavior may be organized, particularly when
  complemented by the excesses and deficits of
  function associated with specific dysfunctions
  (epilepsy, depression, mania).
• One such site is the anterior cingulate
  cortex a candidate for integrating the
  influences of higher cognitive functions and
  emotions -- often viewed as competing
  influences on behavior.

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TRUTH in the BRAIN The NEUROETHOLOGY of BELIEF
Neil Greenberg University of Tennessee Knoxville,
TN USA
QI and COMPLEXITY. Consciousness Reframed
2004....6th International Research Conference.
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TESTING for TRUTH

• Before an organism can be confident in the
  veracity of a percept or belief, it is subjected
  to the tests of correspondence and coherence.
• We will explore evidence of cerebral processes
  that control and integrate these tests.
• Evidence will be considered from neuroethology
  and from case studies of human dysfunction,
  including limbic epilepsy, post-traumatic
  stress disorder, spontaneous confabulation,
  obsessive-compulsive disorder, and schizophrenia.