Download neural mechanisms of animal behavior

AM. ZOOLOGIST, 2:105-115 (1962).
NEURAL MECHANISMS OF ANIMAL BEHAVIOR
KENNETH D. ROEDER
Tufts University
INTRODUCTION
listed above. In addition to the classical
long range neuronal interaction through
spike potentials, local interneuronal action
is possible through neurosecretions and
through subthreshold graded potentials
(Bullock, this volume).
The natural sciences are hierarchical organizations in which each fresh increment
of knowledge revealed by the latest sensors
seems to remove the largest and smallest
hierarchical categories ever further from
THE PROBLEM
our everyday human comprehension. Some
of us may recall those seemly days when
In view of this elaborate neuronal bematter was composed of protons and elechavior
the task of describing animal behavtrons, light traveled in straight lines, and
ior
in
terms
of neuronal mechanisms may
the universe was not expanding, pulsating
be
likened
to
that of describing national
or otherwise acting up. Among the laws
policy
in
terms
of the psychology of human
which were obeyed in those times was the
individuals.
It
is hardly necessary to say
all-or-none law. Sense cells and neurons did
that
it
has
not
been completely accomnot speak unless spoken to, and lapsed into
plished
in
any
single
instance. The neural
inert and unchanging silence until once
mechanism
has
been
mapped
in fragments
more addressed with sufficient intensity.
of
behavior
such
as
the
myotatic
and flexThey had no more behavior than a relay.
ion reflexes of vertebrates, but there is still
The preceding papers of this symposium much obscurity in the manner in which
(see also Bullock, 1958a) have presented a these patterns are coupled to the rest of the
wide repertoire of graded and localized neu- behaving animal.
ronal events that intervene between stimuGranted the complexity of the task, it is
lus, propagated spike potential, and action.
still
worthwhile enquiring why what we
The neuron has been shown to have an
now
know about sensory and synaptic
elaborate intrinsic behavior determined by
events
and nerve impulse transmission has
membrane properties, cell geometry, ion
concentrations, neurohumors, and the tem- not led to a clearer understanding of beporal and spatial configuration of extracel- havior. Bullock (1958b) does not believe
lular impacts upon its soma and dendrites. that "our present physiology of neurons, exIts mode may be highly damped (rapidly trapolated, can account for behavior," and
adapting), undamped (non-adapting), or concludes that "our hope lies in the discovregenerative (endogenously active). These ery of new parameters of neuronal systems."
modes may have their sources at specific Undoubtedly such discoveries will be made,
loci in dendrites or soma, or may be dif- but I feel that our slow progress is due not
fusely spread throughout the neuron. The only to an insufficiency of neurophysiologifinal outcome of this, the spike potential cal information, but also to the point of
propagated in the axon, appears to be a view with which it has been collected, and
simple digital event. Yet the temporal pat- to the manner in which attempts are made
terning of recurring spike potentials can to put it together.
The first encounter with a new biological
convey a great deal more information than
a simple digital code if the spikes impinge mechanism or preparation inevitably elicits
upon another neuron having the properties the question, "how does it work?" and seldom the question, "how does it contribute
Most of the experimental work was made possible
to the system?". The curiosity that prompts
by a grant from the U. S. Public Health Service,
research leads primarily to analysis and
and by earlier support from (he National Science
only rarely to synthesis. Granted that analyFoundation and the Chemical Corps, U. S. Army.
(105)
106
KENNETH D. ROEDER
sis must precede synthesis, if synthesis is the
ultimate objective it should be kept in view
es'cn while the analysis is proceeding. For
example, the squid axon has been the most
popular object of neurophysiological analysis; yet it is hard to find recognition of the
fact that it belongs to a group of motor
fibers supplying the mantle musculature.
fames Bonner (1960) notes this dichotomy of approach in all branches of biology,
and uses the terms "molecular biology" and
"systems biology." He concludes that "the
problem of how the neural network works
has elements which are not intuitively obvious even if one were to know a great deal
about neuro-biochemistry." The logic of
analysis—the molecular approach—seems to
be intrinsically straightforward, and the
problems encountered are mainly technical.
But reconstruction of a closely integrated
system from its components lacks the a priori logic of analysis, and most biologists are
still ill-equipped to use the tools provided
by information theory and systems analysis.
Who does not recall the childhood joy of
taking apart one's first watch, and the dismay and ultimate despair of reassembly
when the screws, springs, and gears were
scattered on the table?
These and other problems standing between neurophysiology and animal behavior would become less formidable if neurophysiologists more frequently took time out
from their experimental analysis of neuronal function to consider its relation to the
behavior of the intact animal. This includes
passive observation of the animal on its
own terms. One of the most important lessons to be learned from the work of Lorenz
and his associates in the field of ethology is
the value of living with the animal under
natural conditions before it is taken into
the laboratory or otherwise restricted by experimentally imposed conditions. Observation requires passivity, patience, and nonintervention, and its rewards are more often
insightful and aesthetic than a source of
quantitative data for publication. A measure of its scientific worth is the degree to
which observation leads to the prediction
of behavior, even when all the criteria for
the prediction cannot be enumerated and
cataloged. The understanding implied by
this ability to predict qualifies the observer
to experiment.
Other difficulties stand in the way of a
closer approach to the general problem. A
few of these will be mentioned briefly. Observation of an animal behaving under
natural conditions leaves the impression
that the animal is completely absorbed or
wholly involved in what it is doing at a
given instant. During courtship much of
the sensori-motor equipment is participating in a single action pattern; in evading a
predator or in food-gathering much of the
same equipment is combined into other
strikingly different but unified action patterns. The behavior patterns are very different in quality but the equipment is
roughly the same. This 'one-mindedness,'
and at the same time this versatility of behavior and its substrate—sense organs, central nervous system, nerves, and musclesis not encountered to the same degree when
attempts are made to reconstruct the role
of other organ systems in the intact animal
from their known physiology. The student
of behavior feels that analysis of the mechanisms destroys this aspect of behavior, but
at the present time the neurophysiologist
can apply his methods in no other way.
Related to this problem is the question
of nerve tracts and centers in the performance of behavior. It is obvious that specific
pathways convey afferent impulses from the
latter to the effectors. Centers are junction
points within the central nervous system
where activity in these pathways shows
some degree of coupling with that of the
peripheral structures. The concept of morphologically localized and specific centers
is necessary to an orderly neurophysiological understanding of behavior, yet it not
only becomes useless but may even be misleading when applied to the more complex
actions of animals. Lashley (1950) searched
in vain over a period of thirty years for evidence of 'the cortical localization of conditioned responses in rats. Von Hoist and
von Saint Paul (1960) stimulated the midbrain region of chickens through indwelling electrodes, and were able to elicit a varietv of complete behavior sequences from
NEURAL MECHANISMS OF BEHAVIOR
the birds' normal repertoire. However, the
mode of behavior released by the stimulus
appeared to be determined by previous activity, surroundings, and the 'mood' of the
bird rather than by the location of the electrodes in the brain. A spatial interpretation of the center concept does not fit these
and many similar studies, but the various
network and field theories proposed to take
its place are still too nebulous to be of
heuristic value.
It is concluded that effective use of neurophysiological information in describing
the mechanisms of behavior is hampered
less by an insufficient knowledge of intraand interneuronal events than by our preoccupation with concepts associated with
the analytic method, and our consequent
failure to arrive at novel viewpoints useful
in the assembly of neurophysiological information.
SOME ATTEMPTS TO RELATE NEURAL
PROPERTIES TO BEHAVIOR
These and other inadequacies of information and concept leave us still very much
at the periphery of the matter. However,
the periphery is wide, leaving room for
many, and it is encouraging to see a growing amount of probing from many angles.
Space does not permit a review, but the
most promising efforts on invertebrates include the work of Huber (see chapter by
Wiersma) on the neural basis of locomotion
and song in crickets, the behavioral cum
cybernetic studies of Mittelstaedt on prey
capture in mantids, and the work of Young
and his associates on brain function and
learning in cephalopods. In the following
pages I shall illustrate three approaches to
the problem from work in our laboratory
at Tufts University.
Central neurons limiting behavior. Speed
of operation is a premium requirement in
behavior connected with the evasion of attacks by predators. Speed requires that the
primary neuronal loop between receptors
and effectors be simple and short, a circumstance that should favor identification of
the neural elements concerned. It is reasonable to suppose that any quantitative
variation in evasive behavior, such as wan-
107
ing of the response on repeated stimulation, is determined by the most labile neuronal event in the chain. The argument is
similar to that applied to rate-limiting reactions in enzyme chains or lemperaturedependent processes.
Cockroaches (Pumphrey and RawdonSmith, 1937; Roeder, 1948; 1953; 1959), locusts (Cook, 1951), dragonfly larvae
(Hughes, 1953; Fielden, 1960), and probably many other insects possess a giant fiber
system in the ventral nerve cord that mediates evasive behavior. Afferent fibers from
an array of mechanoreceptors on the caudal segments converge on the last abdominal ganglion and synapse with a small number of giant fibers. The giants ascend the
abdominal nerve cord and synapse in the
thoracic ganglia with motor neurons supplying the leg muscles. A comparison of
the behavioral response time with the sum
of impulse conduction times and junctional
delays through this system (Roeder, 1959)
suggests that in cockroaches the primary
neuronal loop in evasive behavior consists
of no more than three neurons and two
central synapses (omitting neuromuscular
events).
A puff of air directed at the cerci of a
cockroach that has remained undisturbed
for some time will usually cause it to scuttle
off at high speed. If the stimulus is repeated
several times in quick succession the evasive
response wanes and may disappear entirely.
Even the initial response is quite variable
in different insects and in the same insect
at different times. It would be worthwhile
examining the threshold and intensity of
the evasive response in relation to the circadial changes in activity for which cockroaches are well known.
This lability of the evasive response
makes the situation behaviorally interesting, and one would like to know its neural
basis. Individual segments of the neural
pathway can be checked electrophysiologically for adaptation or fatigue. The axons
involved (cereal nerves, giant fibers, motor
fibers) can be ruled out, since they are capable of transmitting spike potentials for
hours without significant changes in excitability. The receptor cells on the cerci
108
KENNETH D. ROEDER
and the synaptic interaction of their fibers
with the ascending giant fiber system show
some degree of adaptation upon being repeatedly stimulated. However, the time
course of this adaptation is much too long
to account for the waning of the behavioral
response. The temporal stability of the
synapses between cereal nerve and giant
fiber indicates that they play little or no
part in determining the presence or absence of the labile evasive behavior. The
neuromuscular events can be ruled out for
the same reasons. This leaves only the junctions between ascending giant fibers and
motor neurons in the thoracic ganglia.
Attempts to study this synaptic interaction between giants and motor neurons
(Roeder, 1948; 1958) indeed showed that
this process is so labile and subject to failure that it is difficult to perform repeatable
experiments. The tactile stimulation incurred in capturing the cockroach and restraining it for electrode placement may
cause partial or complete transmission failure. Surgical exposure of the ganglion and
interference with its tracheal supply may
contribute in a similar manner. In some
respects the natural instability of this synapse is similar to that induced artificially
in the synapses between cereal nerve and
giant fiber by treating them with the anticholinesterase, DFP. Both neurophysiological and behavioral evidence indicates that
transmission at these labile junctions is dependent both on temporal summation of
ascending volleys in the giant fibers and
upon impulses arriving via descending
pathways from the brain.
This preliminary study has made it clear
that lability of transmission at one junction
in the neuronal loop can determine the
lability of the evasive behavior pattern. Reexamination of this system in the cockroach
and in other insects would be valuable with
present-day electrophysiological methods.
Sensory factors in behavior. The limits
of an animal's ability to respond to a given
stimulus mode can be defined by determining the range of stimuli capable of initiating afferent nerve responses from the relevant receptor field. This determination
does not predict that the animal will overt-
ly react to a given stimulus strength, although a considerable disparity between
sensory performance and known behavior
suggests the need for further study of the
behavior. The need for caution in drawing conclusions about behavior from information about sensory capabilities, and vice
versa, is well illustrated by Tinbergen's
classical study (1935) of the hunting behavior of the wasp, Philanthus Iriangulum.
During the first phase of its hunt for bees
it reacts visually to any bee-like insects, including hover flies, and is completely unresponsive to bee odor. In the second phase
it hovers in the lee of the prospective prey,
and pounces only in the presence of bee
odor. In the third phase stinging is released apparently only if the prey 'feels'
like a bee. Much of our information on
the sensory capabilities of animals is based
on behavioral discrimination tests. Such a
test, if planned without regard for the behavior of Philanthus in its normal context,
could lead to the conclusion that the wasp
is either blind, anosmic, or without tactile
sense.
Another point to be considered in assessing the behavioral role of a sense organ
from a measure of its afferent discharge is
the possibility that efferent fibers and effector mechanisms in the sense organ may
modulate its responsiveness. This type of
feedback mechanism has been studied in
detail in muscle receptor organs (see chapter by Kennedy) and is suspected in other
sense organs. The common practice of recording afferent nerve responses from a
sense organ only after it has been disconnected from the central nervous system
would eliminate efferent impulses of this
kind, and might obscure the normal reporting function of the sense organ.
If allowance is made for these possible
sources of error, the invertebrates offer excellent opportunities to relate sensory input to behavior. When compared with vertebrates their behavior patterns are relatively stereotyped and reproducible when
examined in an appropriate setting, and
their sensory fields usually contain a much
smaller population of receptor cells. The
advantages of these attributes are well
NEUR.U
MECHANISMS OF BEHAVIOR
brought out by the extensive studies of
Dethier and his students on chemoreceptors of flies and their role in hunger and
food-gathering. Here they will be illustrated by reference to the behavioral role
of the tympanic organ found in several
families of moths.
In the Noctuidae the tympanic organs
are situated on the metathorax. The tympanic membranes are directed obliquely
backward and outward into the recess between thorax and abdomen (see Roeder
and Treat, 1957; 1960a and b, for earlier
literature and details). Each tympanic organ contains two acoustic receptor cells (A
cells) and one non-acoustic neuron (B cell)
of uncertain function (Treat and Roeder,
1959). As far as can be discovered, the noctuid moths possess no additional ultrasonic
receptors, so that the total ultrasonic receptor input is represented by spike potentials
in 4 nerve fibers.
This small number of pathways reporting in digital spike sequences to the central
nervous system makes it relatively simple
to decode and to define the total amount of
information received by the moth via this
sense. The tympanic receptors respond to
pure tones ranging from 3 to well over 100
kc/sec. The receptors adapt rapidly to continuous pure tones, and are clearly more responsive to a succession of sound pulses
such as those emitted by echolocating bats.
There appear to be no differences in the
tympanic nerve response to different sound
frequencies, except for decreasing sensitivity at both ends of the frequency range.
A comparison of the afferent response
from a single tympanic organ to short
sound pulses of constant frequency and duration and varying intensity (Fig. 1) reveals
four different forms in which intensity differences can be coded in the spike discharge
of the A receptors. First, spike frequency
(number of spikes per unit time) varies
with sound intensity during the early stages
of the response in either A fiber. Second,
one of the A cells has an acoustic threshold
about 20 db below the other. As stimulus
intensity is increased, first one A cell responds, and then both A cells respond, each
with increasing frequency. This gives the
109
organ two 'ranges' of sensitivity. Third, in
responding to short pulses of moderately
high intensity but constant duration both
A receptors continue to generate spikes for
a significant period after the sound has
ceased. The length of this after-discharge
varies with sound intensity. Fourth, the latent period between the arrival of the sound
and the appearance of impulses at the recording point on the tympanic nerve decreases about 1.5 msec as the sound increases from threshold to maximal. This
change in latency with intensity becomes
greater if the sound pulse has a gradual rise
time, as is the case with a bat cry.
Assuming that the moth possesses appropriate central mechanisms for differentiating these various types of afferent discharge, it can be concluded that the first
and second types of intensity discrimination would permit a moth with a single
tympanic organ to distinguish between serially presented sounds of varying loudness,
irrespective of pulse length. Sound pulses
of different length could also be distinguished, although they would be distorted
by rapid adaptation of the receptors. The
third type, that depending upon an afterdischarge, would confuse pulse length with
intensity. The fourth type, that depending
upon latency, would be unavailable to a
moth with a single ear.
It has been shown (Roeder and Treat,
19G1 a) that the tympanic organs are somewhat directional, responding to a click of
constant intensity presented on the near
side at about twice the distance as compared with the response when the click is
presented on the far side of the body. Assuming central mechanisms capable of making a simultaneous comparison between
right and left afferent responses, all four
forms of intensity discrimination would be
theoretically available to a moth possessing
both tympanic organs, although pulse
length and intensity would still be confused by the third form. Furthermore, any
or all of these forms of intensity discrimination could provide the moth with a rough
indication of the direction of a relatively
faint sound, i.e., whether its source lay to
the right or left of the moth. Directional
no
KENNETH D. ROEDER
FIG. 1. Tympanic nerve responses (lower traces) of
Noctua c-nigrum to a 70 kc. sound pulse recorded
simultaneously (upper traces) by a Granith microphone placed near the preparation. The number in
each frame indicates the sound intensity in decibels
above a level (0) close to the threshold of the most
sensitive A receptor. The less sensitive A receptor
responds first in the 25 db. record (overlapping
spikes). The larger spikes appearing in some records belong to the B cell. Vertical lines are 4 msec,
apart. (From Roeder and Treat, 1961ft,Am. Scientist.)
information about loud sounds would not
be available, since the tympanic receptors
saturate at sound intensities approximately
40 db above threshold. These conclusions
were confirmed by binaural recordings of
the afferent responses of Noctuids to freeflying bats in the field.
Thus, the small number of receptor cells
in the tympanic organ makes it possible to
define with some precision the total amount
of impulse-coded information available to
the moth through this sense modality. The
fact that the organ has obvious survival
value in enabling the moth to detect and
evade hunting bats (Roeder and Treat,
1960) makes it doubly enticing to relate
this afferent information to central nervous
events and to the moth's consequent behavior.
Attempts to trace second order connet-
tions made by the tympanic nerves in the
central nervous system have not yet been
successful, but will be pursued further. The
erratic dodging and diving shown by moths
when approached by feeding bats is well
known. Attempts are being made to study
these manuevers more precisely by exposing free-flying moths in the field to a source
of simulated bat cries. So far, the behavioral studies have confirmed the sensory
findings. High intensity sounds cause
abrupt diving and a variety of other erratic
changes in flight pattern which lack any obvious directional component. Low intensity sounds cause a turning-away from the
sound source accompanied by an increase
in flight speed. It is hoped that, by varying repetition rate, frequency and other
parameters of the artificial sound pulse, it
will be possible to find whether only some
NEURAL MECHANISMS OF BEHAVIOR
or all of these forms of intensity coding determine the evasive pattern of the moth.
Endogenous nerue activity and behaxriov.
Endogenous or spontaneous nerve activity
is here defined as on-going or repetitive
neural events that have their origin in the
internal states of the animal. External
stimuli impinging on the sense organs may
modulate endogenous activity, but by definition do not cause it. Repetitive activity
in receptor cells completely isolated from
their normal sources of stimulation, or in
central neurons following severance of all
afferent pathways, is designated as endogenous.
Endogenous activity in receptor cells and
central neurons is widespread among the
invertebrates. It was first examined electrophysiologically in arthropods by Adrian
(1931) and Prosser (1934). Its neuronal basis and the forms it may take are discussed
in this volume by Kennedy, Van der Kloot,
and Bullock.
At first glance it might seem that endogenous activity originating in a receptor or
ganglion cell which gives rise to propagated
spike potentials in its axon would make the
unit 'noisy' as a communications channel,
and thereby tend to obscure discrete neural
signals. However, the signalling capacity
of excitable cells is actually improved in
certain respects by the presence of endogenous activity. First, the threshold to extrinsic stimuli becomes reduced to its vanishing point, since any external change,
however small, may be expected to alter
the firing rate. Second, the external stimulus can alter the firing rate in two directions, causing either an increase or a decrease in the endogenous rhythm. Neurons,
which are active only when their threshold
is surmounted by a stimulus of sufficient intensity, and endogenously active neurons,
may be likened respectively to meters, one
of which has the zero point at one end of
the scale, and the other the zero at the center of the scale. The first can provide a
quantitative measure of current flow only
in one direction, while the second can measure changes in current flowing in either direction.
Ethological studies (Lorenz, 1950; Tin-
111
bergen, 1951) conclude that many forms of
animal behavior contain an endogenous
component responsible for appetitive or
search activities and a taxis component
added when the appetitive movements
carry the animal within the range of suitable releasers. It seems reasonable to suppose that the endogenous component responsible for appetitive behavior is a manifestation of endogenous nerve activity.
However, the presence of endogenous nerve
activity can be established only if the animal is deprived of afference. This condition is so difficult to achieve experimentally, and so rigorous from the behavioral
point of view, that it is not easy to devise
an experiment to demonstrate a connection between endogenous nerve activity and
appetitive behavior (see Roeder, 1955, for
a summary of earlier attempts to solve this
problem). The courtship behavior of the
male praying mantis suggested one way of
meeting this difficulty.
The adult male praying mantis (Mantis
religiosa L. or Heirudida tenuidcntala Saussure) makes a slow, visually steered approach to the female. During this phase
copulatory movements of the abdomen (Sshaped bending) are minimal or absent.
When the pair are about one length apart
the male mounts the female in a quick
leap, clasps her at the base of the prothorax, and within a few minutes makes copulatory movements of increasing intensity
leading to eventual copulation. Sometimes
the male is attacked by the female and
eaten during his approach. His head is usually consumed first, and this releases in the
male vigorous and continuous copulatory
movements and a curious pattern of rotary
locomotion never observed in an intact insect. These activities often carry the male
into the normal mating position even while
he is being eaten, and copulation usually
takes place more rapidly than is the case
when the male is intact. Artificial decapitation of a mature male, or removal of the
subesophageal ganglion, produces the same
effect in the absence of a female, and rotary locomotion and copulatory movements
continue for days. Encounters between
headless males and objects the size and
112
KENNETH D. ROEDER
FIG. 2. Sexual behavior in the mantis, Heirudula
tennidenlata. (A) Mating pair in which the male
has not been attacked by the female. The presence
of the housefly is incidental. (B) Mating pair in
which the male was attacked and partially eaten as
he attempted to mount the female. (C) and (D)
Female consuming head and part of the prothorax
of a male attacked during his final approach. Subsequent to these pictures this male was able to gain
a foothold on the wings of the female, and eventually copulated. In (C) note the bending of the
male abdomen characteristic of the copulatory posture. (Modified from Roeder, Tozian and Weiant,
1960, J. Insect Physio!.)
shape of females lead to clasping and attempted copulation (Roeder, 1935). Portions of the behavior described above are
seen in the photographs of Fig. 2.
Two aspects of this behavior are relevant
to the present matter. First, the rotary locomotion and abdominal movements can be
classed as appetitive activities with adaptive value in that they increase the chances
of fertilization in spite of the cannibalistic
tendency of the female. Second, locomotion is mediated by local nerve centers in
the thoracic ganglia, and copulatory movements are controlled entirely by nerve activity in the last abdominal ganglion. These
activities in local centers are normally suppressed by inhibitory centers in the subeso-
phageal ganglion. The rotary locomotion
has never been observed in intact males,
while the copulatory movements are normally manifest only when male and female
are in physical contact, and then rarely
with the intensity observed after decapitation. Evidence that the copulatory movements are endogenous in origin was obtained in the following way (Roeder, Tozian, and Weiant, I960).
The last abdominal ganglion of a male
mantis was exposed and silver recording
electrodes were placed under the phallic
nerve. This nerve supplies much of the
musculature of the phallomeres and terminal abdominal region. The phallic nerve
was severed distally, limiting activity re-
NEURAL MECHANISMS OF BEHAVIOR
113
FIG. 3. Efferent nerve impulses in nerve IX (upper
trace) and in the phallic branch of nerve X (lower
trace) of a male cockroach, Periplaneta americana
L. (A) The last abdominal ganglion is still connected to the nerve cord. (B) 4 minutes, and (C)
10 minutes after transection of the nerve cord and
neural isolation of the last abdominal ganglion.
Additional motor units have become spontaneously
active in both nerves, but are not synchronized with
each other. The slower rhythmic nature of the
bursts of motor impulses is not apparent in these
short records. (After Roeder, To/.ian, and Weiant,
I960, J. Insect Physiol.)
corded by the electrodes to efferent impulses. Local afference was eliminated by
cutting all other nerves leaving the ganglion. This left the abdominal nerve cord
as the only connection between the last abdominal ganglion and the rest of the nervous system and sense organs. The level of
efferent activity in the phallic nerve was
noted over a period of about 30 minutes.
When this became relatively constant the
abdominal nerve cord was severed just
above the ganglion. This eliminated the
final pathway over which afferent impulses
might reach the ganglion, and at the same
time removed it from the influence of the
inhibitory center in the subesophageal ganglion. Within 3 to 15 minutes efferent activity that would normally have reached
the phallic musculature increased several
fold, both in number of spikes in individual motor fibers and in the number of motor units active (Fig. 3). This increased
activity continued for hours, and often
showed a complex patterned rhythmicity
that might have been expected to produce
rhythmic muscular movements if the peripheral connections of the nerve had been
intact. A similar release of motor nerve activity occurred if the insect was merely decapitated.
These experiments demonstrate that
both copulatory movements and endogenous activity of motor neurons supplying
the abdominal appendages are subject to
control by inhibition from the subesophageal ganglion. This strongly suggests that
copulatory movements have their origin in
the endogenous activity of neurons in the
114
KENNETH D. ROEDER
last abdominal ganglion, although direct
proof of this is lacking owing to the impossibility of severing all afferent pathways
while leaving intact the efferent nerve fibers
necessary to produce the behavior. Of
course, this does not mean that copulation
can be accomplished merely through the
agency of endogenous activity. Afferent impulses generated through contact with the
female most certainly modulate and steer
endogenous activity in order to achieve
coupling, but they have not been investigated.
In cockroaches, there is a similar neurophysiological situation. Endogenous efferent activity is released when segmental ganglia are isolated from the rest of the nervous system (Weiant, 1956; Roeder, Tozian,
and Weiant, 1960). The neuropharmacology of the endogenously active neurons and
the subesophageal inhibitory system has
been examined (Milburn, Weiant and Roeder, 1960). The latter showed that extracts
of the corpus cardiacum released motor
nerve activity in the last abdominal ganglion of cockroaches in a reversible but
otherwise similar manner to transection of
the nerve cord.
In the experiments with cockroaches the
neurophysiological picture is similar to that
found in the praying mantis, yet decapitation of male cockroaches leads only to discoordinated movements of abdomen and
phallomeres and not to active and effective
attempts to copulate. In view of the absence of sexual cannibalism in cockroaches,
full-fledged copulatory behavior following
decapitation could have little or no value
in species survival. The appearance of endogenous nerve activity in a segmental ganglion when it is isolated from the rest of
the nervous system may have significance in
the phylogenetic history of the arthropod
nervous system. Perhaps the super-position
and elaboration of intersegmental inhibitory pathways was a major factor in the
evolution of the closely knit arthropod
nervous system from that of an annelid-like
ancestor having a series of similar and relatively autonomous segmental ganglia. Coordination of local rhythmic activities into
the highly integrated and diverse action
patterns of arthropods may have been accomplished by the addition of this permissive mechanism, that is, by controlled release of local activity from inhibitory effects of extrasegmental origin. In the male
mantis this general method of segmental
regulation may have acquired secondary
adaptive significance through the cannibalistic tendency of the female.
This suggests that inhibition of extrasegmental origin might be expected to play a
large part in the interaction of different
nerve centers in arthropods. This seems to
be the case. Locomotion in mantids (Roeder, 1937) and locomotion and song production in crickets (Huber, I960; see also
Wiersma, this volume) are regulated
through inhibitory mechanisms, sometimes
with one inhibitory system acting upon another. On the sensory side Ruck (1961) has
shown that photic excitation of the ocellar
photoreceptors in certain insects inhibits
endogenous spike activity in the second order afferent fibers of the ocellar nerve. In
fully dark-adapted ocelli intermittent endogenous activity may break out in the receptor cells, producing intermittent inhibition of the endogenous activity in the second order fibers. The role of inhibition in
arthropod motor and proprioceptor mechanisms is discussed in this volume by Hoyle
and by Van der Kloot.
CONCLUSIONS
These three examples were chosen from
the growing literature on the relation of
neurophysiology to animal behavior partly
because of my familiarity with them and
partly because they serve to illustrate some
of the gains and some of the road blocks to
progress in this field. On the credit side
they supplement what has been amply illustrated elsewhere in this symposium, i.e.,
that invertebrates are promising subjects
for relating nerve function to behavior because of accessibility and relative simplicity
of their nervous systems combined with
relative fixity and reproduceability of their
behavioral patterns. On the debit side the
experiments show that proper use of the
neurophysiological information already at
hand as well as the planning of new experi-
NEURAL MECHAIMISMS OF BEHAVIOR
merits is hampered by the lack of adequate
conceptual frameworks for dealing with
events in the core of the nervous system.
Old standbys, such as the reflex and the
morphological center, have become peripheral in their significance, but the new
data on graded inter- and intraneuronal interactions deal primarily with nerve units
rather than nerve populations, and therefore cannot alone fill the gap. It cannot be
said whether the needed assistance will
come primarily from the new and powerful
concepts of information theory, or from
zoological or physiological sources. Nevertheless, the present status of the search for
a neural basis of behavior makes it an exciting field of research endeavor.
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