402 
HOW THE CATFISH TRACKS ITS PREY: AN INTERACTIVE "PIPELINED" 
PROCESSING SYSTEM MAY DIRECT FORAGING VIA RETICULOSPINAL NEURONS. 
Jagmeet S. Kanwal 
Dept. of Cellular & Structural Biology, Univ. of Colorado, Sch. of 
Medicine, 4200 East, Ninth Ave., Denver, CO 80262. 
ABSTRACT 
Ictalurid catfish use a highly developed gustatory system to 
localize, track and acquire food from their aquatic environment. 
The neural organization of the gustatory system illustrates well 
the importance of the four fundamental ingredients 
(representation, architecture, search and knowledge) of an 
"intelligent" system. In addition, the "pipelined" design of 
architecture illustrates how a goal-directed system effectively 
utilizes interactive feedback from its environment. Anatomical 
analysis of neural networks involved in target-tracking 
indicated that reticular neurons within the medullary region of 
the brainstem, mediate connections between the gustatory 
(sensory) inputs and the motor outputs of the spinal cord. 
Ele ctrophysiological analysis suggested that these neurons 
integrate selective spatic-temporal patterns of sensory input 
transduced through a rapidly adapting-type peripheral filter 
(responding tonically only to a continuously increasing stimulus 
concentration ). The connectivity and response patterns of 
reticular cells and the nature of the peripheral taste response 
suggest a unique "gustation-seeking" function of reticulospinal 
cells, which may enable a catfish to continuously track a 
stimulus source once its directionality has been computed. 
INTRODUCTION 
Food search is an example of a broad class of behaviors 
generally classified as goal-directed behaviors. Goal-directed 
behavior is frequently exhibited by animals, humans and some 
machines. Although a preprogrammed, hard-wired machine may achieve 
a particular goal in a relatively short time, the general and 
heuristic nature of complex goal-directed tasks, however, is best 
exhibited by animals and best studied in some of the less advanced 
animal species, such as fishes, where anatomical, electro- 
physiological and behavioral analyses can be performed relatively 
accurately and easily. 
Food search, which may lead to food acquisition and ingestion, 
is critical for the survival of an organism and, therefore, only 
highly successful systems are selected during the evolution of a 
species. The act of food search may be classified into two distinct 
phases, (i) orientation, and (ii) tracking (navigation and homing). 
In the channel catfish (the animal model utilized for this study), 
locomotion (swimming) is primarily controlled by the large forked 
caudal fin, which also mediates turning and directional swimming. 
American Institute of Physics 1988 
403 
Both these forms of movement, which constitute the essential 
movements of target-tracking, involve control of the 
hypaxial/epiaxial muscles of the flank. The alternate contraction 
of these muscles causes caudal fin undulations. Each cycle of the 
caudal fin undulation provides either a symmetrical or an 
asymmetrical bilateral thrust. The former provides a net thrust 
forward, along the longitudinal axis of the fish causing it to move 
ahead, while the latter biases the direction of movement towards the 
right or left side of the fish. 
,,  HRP injection site 
  recording site 
..................................................................................... NEURODIOLOGY ...... I .................................... 
FEEDING BEHAVIOR MUSCLE SET MOTOR POOLS PREMOTOR NEURONS I GUSTATORY INPUTS 
Food Search Flank and Caudal Reticular I Facial Lobe 
Tail Fin Spinal Cord . ............ tl Formation - ......................... 
I Muscles i ..................................................................................................... 
Pick Up 
Selective 
Ingestion 
Flank 
Musculature 
Jaw Muscles 
Oral 'nd 
Pharyngeal 
Musculature 
 
Rostral Rettcular Facial Lobe 
Spinal Cord . ........... 0 Formation . .......................... 0 
Facial and/or . ............................................................................ l 
Trieminal 
Motor Nucleus 
Yaal Motor 
Nuclei 
Vagal Lobe 
I ntrt nsic 
I nterneurons 
Vagal Lobe 
Fig. I. Schematic representation of possible pathways for the 
gustatory modulation of foraging in the catfish. 
4O4 
Ictalurid catfishes possess a well developed gustatory system 
and use it to locate and acquire food from their aquatic 
environment l, 2,3. Behavioral evidence also indicates that ictalurid 
catfishes can detect small intensity (stimulus concentration) 
differences across their barbels (interbarbel intensity 
differences), and may use this or other extraoral taste information 
to compute the directionality in space and track a gustatory 
stimulus source 1. In other words, based upon the analysis of 
locomotion, it may be inferred that during food search, the 
gustatory sense of the catfish influences the duration and degree of 
asymmetrical or symmetrical undulations of the caudal fin, besides 
controlling reflex turns of the head and flank. Since directional 
swimming is ultimately dependent upon movement of the large caudal 
fin it may be postulated that, if the gustatory system is to 
coordinate food tracking, gustato-spinal connections exist upto the 
level of the caudal fin of the catfish (fig. 1). 
The objectives of this study were (i) to reconsider the 
functional organization of the gustatory system within the 
costraints of the four fundamental ingredients (representation, 
architecture, search and knowledge) of a naturally or artificially 
"intelligent" agent, (ii) to test the existence of the postulated 
gustato-spinal connections, and (iii) to de lineate as far as 
possible, using neuroanatomical and electrophysiological techniques, 
the neural mechanism/s involved in the control of goal-directed 
(foraging) behavior. 
ORGANIZATIONAL CONSIDERATIONS 
I. REPRESENTATION 
Representation refers to the translation of a particular task 
into information structures and information processes and determines 
to a great extent the efficiency and efficacy with which a solution 
to the task can be generated4. The elaborate and highly sensitive 
taste system of an ictalurid catfish consists of an extensive array 
of chemo- and mechanosensory receptors distributed over most of the 
extraoral as well as oral regions of the epithelium2,5.. 
Peripherally, branches of the facial nerve (which innervates all 
extraoral taste buds resoond to a wide range of stimulus (amino 
acids) concentrationsO,7, .e. from 10-9M to 10-3M. The taste 
activity however, adapts rapidly (phasic response) to ongoing 
stimulation of the same concentration (Fig. 2) and responds 
tonically only to continuously increasing concentrations of stimuli, 
such as L-arginine and L-alanine. 
rp ros 
Fig. :fl. Integrated, facial taste recordings to continuous appli- 
cation of amine acids to the palate and nasal barbel showing the 
phasic nature of the taste responses of the ramus palatinus (rp) 
and ramus ephthalmicus superficialis (res), respectively. 
.L-ALA 
1( 4 
.L-ARG 
4O5 
Gustatory information from the extraoral and oral epithelium is 
"pipelined" into two separate subsystems, facial and 
glossopharyngeal-vagal, respectively. Each subsystem processes a 
subset of the incoming information (extraoral or oral) and 
coordinates a different component of food acquisition. Food search 
is accomplished by the extraoral subsystem, while selective 
ingestion is accomplished by the oral subsystem 2 (Fig. 3). The 
extraoral gustatory information terminates in the facial lobe where 
it is represented as a well-defined topographic map 9, l0 , while the 
oral information terminates in the adjacent vagal lobe where it is 
represented as a relatively diffuse map ll. 
II. ARCHITECTURE 
The information represented in an information structure 
eventually requires an operating frame (architecture) within which 
to select and carry out the various processes. In ictalurid catfish, 
partially processed information from the primary gustatory centers 
(facial and vagal lobes) in the medullary region of the brainstem 
converges along ascending and descending pathways (Fig. 4). One of 
the centers in the ascending pathways is the secondary gustatory 
nucleus in the isthmic region which is connected to the 
corresponding nucleus of the opposite side via a large 
commissurel2,13. Facial and vagal gustatory information crosses 
over to the opposite side via this commissure thus making it 
possible for neurons to extract information about interbarbel or 
interflank intensity differences. _lthough neurons in this region 
are known to have large receptive fieldsl4, the exact function of 
this large commissural nucleus is not yet clearly established. 
It is quite clear, however, that gustatory information is at 
first "ipelined" into separate regions where it is processed in 
parallel 5 before converging onto neurons in the ascending (isthmic) 
and descending (reticular) processors as well as other regions 
within the medulla. The "pipelined" architecture underscores the 
need for differential processing of subsets of sensory inputs which 
are consequently integrated to coordinate temporal transitions 
between the various components of goal-directed behavior. 
III. SEARCH 
An important task underlying all "intelligent" goal directed 
activity is that of search. In artificial systems this involves 
application of several general problem-solving methods such as 
means-end analysis, generate and test methods and heuristic search 
methods. No attempt, as yet, has been made to fit any of these 
models to the food-tracking behavior of the catfish. However, 
behavioral observations suggest that the catfish uses a 
combinatorial approach resulting in a different yet optimal foraging 
strategy each time 3. 
What is interesting about biological models is that the 
intrinsic search strategy is expressed extrinsically by the behavior 
of the animal which, with a few precautions, can be observed quite 
easily. In addition, simple manipulations of either the animal  or 
its environment can provide interesting data about the search 
4O6 
Fig. 3. 
SENSORY 
FISH BEHAVIORAL 
INPUT BRAI N OUT PUT 
__ arp ix 
b 
ora U 
d X 
oChre I t food search 
and 
pmck uP 
vaal I 
lobe  ..... select,ve 
neston 
i ? 
L._ 
VII 
IX 
x 
Fig. 4. 
4O7 
strategy/ies being used by the animal, which in turn can highlight 
some of the computational (neuronal) search strategies adopted by 
the brain e.g. the catfish seems to minimize the probability of 
failure by continuously interacting with the environment so as to be 
able to correct any computational or knowledge-based errors. 
IV. KNOWLEDGE 
If an "intelligent" goal-directed system resets to zero 
knowledge before each search trial, its success would depend 
entirely upon the information obtained over the time period of a 
search. Such a system would also require a labile architecture to 
process the varying sets of information generated during each 
search. For such a system, the solution space can become very large 
and given the constraints of time (generally an important criterion 
in biological systems) this can lead to continuous failure. For 
these reasons, knowledge becomes an important ingredient of an 
"intelligent" agent since it can keep the search under control. 
For the gustatory system of the catfish too, randomly 
accessable knowledge, in combination with the immediately available 
information about the target, may play a critical role in the 
adoption of a successful search strategy. Although a significant 
portion of this knowledge is probably learned, it is not yet clear 
where and how this knowledge is stored in the catfish brain. The 
reduction in the solution space for a catfish which has gradually 
learned to find food in its environment may be attributed to the 
increase in the amount of knowledge, which to some extent may 
involve a restructuring of the neural networks during development. 
EXPERIMENTAL METHODS 
The methods employed for the present study are only briefly 
introduced here. Neuroanatomical tracing techniques exploit the 
phenomenon of axonal transport. Crystals of the enzyme, horseradish 
peroxidase (HRP) or some other substance, when injected at a small 
locus in the brain, are taken up by the damaged neurons and 
transported anterogradely and retrogradely from cell bodies and/or 
axons at the injection site. In the present study, small 
superficial injections of HRP (Sigma, Type VI) were made at various 
loci in the facial lobe (FL) in separate animals. After a survival 
period of 3 to 5 days, the animals were sacrificed and the brains 
sectioned and reacted for visualization of the neuronal tracer. In 
this manner, complex neural circuits can be gradually delineated. 
Electrophysiological recordings from neurons in the central 
nervous system were obtained using heat-pulled glass micropipettes. 
These glass electrodes had a tip diameter of approximately 1 m and 
an impedance of less than 1 megohm when filled with an electrolyte 
(SM KC1 or 5M Nacl). 
Chemical stimulation of the receptive fields was accomplished 
by injection of stimuli (amino acids, amino acid mixtures and liver 
or bait-extract solutions) into a continuous flow of well-water over 
the receptive epithelium. Tactile stimulation was performed by 
gentle strokes of a sable hair brush or a glass probe. 
4O8 
EXPERIMENTAL OBSERVATIONS 
Injections of HRP into the spinal cord labelled two relevant 
populations of cells, (i) in the ipsilateral reticular formation at 
the level of the facial lobe (FL), and (ii) a few large scattered 
cells within the ipsilateral, rostral portion of the lateral lobule 
of the FL (Fig. 5). Injection of HRP at several sites within the FL 
resulted in the identification of a small region in the FL from 
where anterogradely filled fibers project to the reticular formation 
(Fig. 5). Superimposition of these injection sites onto the 
anatomical map of the extraoral surface of the catfish indicated 
that this small region, within the facial lobe, corresponds to the 
snout region of the extraoral surface. 
FACIO-RETICULAR PROJECTIONS 
FACIO- & RETICULO -SPINAL PROJECTIONS 
1 
injection site 
I SpC 
,-, 
 .'"-_';'i ' 
2 
injection site 
3 
CB =cerebellum 
LL =lateral line lobe 
Fig. 5. Schematic chartings showing 
labelled-cell bodies(squares) and fibers 
transverse sections through the medulla. 
(dots) in 
4O9 
FL = facial lobe 
 RF = reticular formation 
 !  SpC = spinal cord 
FLANK SNOUT 
Fig. 6A. 
WATER SQUIRT -HEAD 
GLIDING TOUCH -FLANK 
II! !111 I I I III 111111 ! IJ. iLl. _1. It I I!_ III 
ill II!i  Jill ill dl 11 
LIVER ERA -SND 
AHINO ACID HIURE  
(Receptive (Sample unit responses) 
' CONTROL ' 
,,I.,,h,l],il.l,ll,,[,lllJ,llll[,. !,I]!:, I lil. I, iI...l,.l I....I,..._L, .]]l 
AlIINO ACID I11XTURE  -SNOrt1" 
Fig. 6B. 
410 
Multiunit electrophysiological recordings from various 
anteroposterior levels of the reticular formation indicated that the 
snout region (upper lip and proximal portion of the maxillary 
barbels) of the catfish project to a disproportionately large region 
of the reticular formation along with a mixed representation of the 
flank (Fig. 6A). 
Single unit recordings indicated that some neurons have 
receptive fields restricted to a bilateral portion of the snout 
region, while others had large receptive fields extending over the 
whole flank or over an anteroposterior half of the body (Fig. 6B). 
DISCUSSION 
The experimental results obtained here suggest that facial lobe 
projections to the reticular formation form a functional connection. 
The reticular neurons project to the spinal cord and, most likely, 
influence the general cycle of swimming-related activity of 
motoneurons within the spinal cord 16. 
The disproportionately large representation of the snout region 
within the medullary reticular formation, as determined 
electrophysiologically, is consistent with the anatomical data 
indicating that most of the fibers projecting to the reticular 
formation originate from cells in that portion of the facial lobe 
where the snout region is mapped. The lateral lobule of the spinal 
cord has a second pathway which projects directly into the spinal 
cord upto the level of the anterior end of the caudal fin and may 
coordinate reflexive turning. 
The significance of the present results is best understood when 
considered together with previously known information about the 
anatomy and electrophysiology of the gustatory system. The 
information presented above is used to propose a model (Fig. 7) for 
a mechanism that may be involved during the homing phase of target 
tracking by the catfish. During homing, which refers to the last 
phase of target-tracking during food search, it may be assumed that 
the fish is rapidly approaching its target or moving through a steep 
signal intensity (stimulus concentration) gradient. The data 
presented above suggest that a neuronal mechanism exists which helps 
the catfish to lock on to the target during homing. This proposal 
is based upon the following considerations: 
I. Owing to the rapidly adapting response of the peripheral filter, 
a tonic level of activity in the facial lobe input can occur only 
when the animal is moving through an increasing concentration 
gradient of the gustatory stimulus. 
2. Facial lobe neurons, which receive inputs from the snout region, 
project to a group of cells in the reticular formation. Activity in 
the facio-reticular pathway causes a suppression in the spontaneous 
activity of the reticular neurons. 
3. Direct and/or indirect spinal projections from the reticular 
neurons are involved in the modulation of activity of those spinal 
motoneurons which coordinate swimming. Thus, it may be hypothesized 
that during complete suppression of activity in a specific reticulo- 
spinal pathway, the fish swims straight ahead, but during excitation 
411 
of certain reticulospinal neurons the fish changes its direction as 
dictated bY the pattern f activatin' i 
Fig. 7. The snout region of 
the catfish has secial si-ificance 
because of its extensive 
represetto the 
formation. In same the fish makes a i ..',:] ' '  .",,". 
random or computational error, while .-'/ ':'ff I : '"'. 
approaching its target, the snout is -"/ /  .."N '"': 
the first region to move out of the /: 
Thus, the spinal moroneurons, teleologically speaking, "seek" a 
statory stimulus in order to suppress activity of certain 
reticulospinal neurons, which in turn reduce variations in the 
pattem of activity of simming-related spinal moroneurons. 
tccordingly, in a situation where the fish is rapidly approaching a 
target, ie. under the specific conditions of a continuously rising 
stimulus concentration at the snout region and an absence of a 
stimulus intensity difference across the barbels, there is a locking 
of the movement of the body (of the fish) towards the stationary or 
moving target (food or prey). 
It should be pointed out, however, that the empirical data 
available so far, only offers clues to the target-tracking mechanism 
proposed here. Clearly, more research is needed to validate this 
proposal and to identify other mechanisms of target-tracking 
utilized by this biological system. 
This research was supported in part by NIH Grant NS15258 to 
T.E. Finger. 
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