How does the toad's visual system discriminate different worm-like stimuli?

Behavioral experiments show that toads exhibit stimulus- and locus-specific habituation. Different worm-like stimuli that toads can discriminate at a certain visual location form a dishabituation hierarchy. What is the neural mechanism which underlies these behaviors? This paper proposes that the toad discriminates visual objects based on temporal responses, and that discrimination is reflected in different average neuronal firing rates at some higher visual center, hypothetically anterior thalamus. This theory is developed through a large-scale neural simulation which includes retina, tectum and anterior thalamus. The neural model based on this theory predicts that retinal R2 cells play a primary role in the discrimination via tectal small pear cells (SP) and R3 cells refine the feature analysis by inhibition. The simulation demonstrates that the retinal response to the trailing edge of a stimulus is as crucial for pattern discrimination as the response to the leading edge. The new dishabituation hierarchies predicted by this model by reversing contrast and shrinking stimulus size need to be tested experimentally.     

Local non-linear interactions in the visual cortex may reflect global decorrelation

The classical receptive field in the primary visual cortex have been successfully explained by sparse activation of relatively independent units, whose tuning properties reflect the statistical dependencies in the natural environment. Robust surround modulation, emerging from stimulation beyond the classical receptive field, has been associated with increase of lifetime sparseness in the V1, but the system-wide modulation of response strength have currently no theoretical explanation. We measured fMRI responses from human visual cortex and quantified the contextual modulation with a decorrelation coefficient (d), derived from a subtractive normalization model. All active cortical areas demonstrated local non-linear summation of responses, which were in line with hypothesis of global decorrelation of voxels responses. In addition, we found sensitivity to surrounding stimulus structure across the ventral stream, and large-scale sensitivity to the number of simultaneous objects. Response sparseness across voxel population increased consistently with larger stimuli. These data suggest that contextual modulation for a stimulus event reflect optimization of the code and perhaps increase in energy efficiency throughout the ventral stream hierarchy. Our model provides a novel prediction that average suppression of response amplitude for simultaneous stimuli across the cortical network is a monotonic function of similarity of response strengths in the network when the stimuli are presented alone.     

A feedforward model of suppressive and facilitatory habituation effects

 Simple exposure to repeatitive stimulation is known to induce short-term learning effects across a wide range of species. These effects can be both suppressive and facilitatory depending on stimulus conditions: repeatitive presentation of a weak stimulus decreases the strength of the response (habituation), whereas presentation of a tonic stimulus following a series of weak stimuli transiently increases the response strength (dishabituation). Although these phenomena have been comprehensively characterized at both behavioral and cellular levels, most existing models of nonassociative learning focus exclusively on the suppressive or facilitatory changes in response, and do not attempt to relate cellular events to behavior. I propose here a feedforward model of habituation effects that explains both suppressive and facilitatory changes in response relying on the interaction between excitatory and inhibitory processes that develop in parallel on two different timescales. The model's properties are used to explain the rate sensitivity property of habituation and recovery and stimulus dishabituation. Received: 1 June 2001 / Accepted in revised form: 4 December 2001     

Neuronal responses are differentially affected by the polarity of tectal DC stimulation in the toad Bufo bufo

Male toads were tested behaviourally for their prey catching responses to worm-like stimuli before being prepared for visual unit and slow potential shift (SPS) recording from the optic tectum. The neuronal responses of toads to a prey-like visual stimulus reflected their motivational tendency prior to operations. One second of DC stimulation to the tectum was followed by an SPS of reversed polarity during which time a visual prey-like stimulus was presented. A negative SPS following positive DC stimulation was associated with enhanced neuronal responses to a visual stimulus. The positive SPS that followed negative stimulation was associated with a decline in neural responses below background when a visual stimulus was additionally given. The SPS was largely a result of DC stimulation that interacted with the motivational tendency to produce enhanced neuronal responses, while the potential was negative and vice versa.     

Stimulus size selectivity and receptive field organization of ectostriatal neurons in the pigeon

The avian ectostriatum is the telencephalic recipient zone of the tectofugal pathway, which may be homologous to the colliculo-pulvinar-cortical pathway in mammals. The present paper studies the visual response properties and receptive field organization of ectostriatal cells in pigeons with extracellular recording and computer mapping techniques. The results indicate that 90% of ectostriatal cells prefer forward, downward and upward motion of visual stimuli at velocities in the range of 16-128 degrees s(-1). They respond optimally to small stimuli (1-4 degrees visual angle), mostly preferring a target of 2 degrees. Most cells (78.8%) have one excitatory receptive field that usually possesses one or two hotspots, some cells (13.5%) have two excitatory receptive fields each having one or two hotspots, and a few cells (7.7%) have one excitatory receptive field with an unresponsive region in the center. An inhibitory receptive field is not found surrounding the excitatory receptive field in the ectostriatal cells examined. These response properties and receptive field organization may reflect the possible roles of the ectostriatum in stimulus discrimination and visual cognition.     

Configurational prey-selection by individual experience in the toadBufo bufo

Summary The habituation method was used to investigate the toad's ability to discriminate between two dimensional prey dummies of different shapes and patterns: If immediately following habituation of the prey-catching orienting behavior to a dummy form A, prey-catching responses are elicited when another form B is presented, it can be concluded that the toad is able to discriminate between the two patterns. The results show that toads are able to discern detailed structures within the outline limits of a 5 mm× 20 mm worm-like shape, on the basis of individual experience (stimulus specific habituation). In particular the results demonstrate that triangular stimulus patterns moved with a horizontal acute angle leading increase the releasing value of prey features whereas separate additional dots moved simultaneously may reduce the prey features of an optimal prey dummy. Dots, stripes and acute angles obviously have a significant effect in theexperience governed pattern discrimination of prey for toadsBufo bufo.Supported by grants of the Deutsche Forschungsgemeinschaft Ew 7/6     

A model of the neural mechanisms responsible for pattern recognition and stimulus specific habituation in toads

A neural model of the mechanisms possibly responsible for stimulus-specific habituation in toads is proposed. The model follows the hypothesis that preypredator recognition is performed by command units as a result of retina-tectum-pretectum interaction. The model allow us to study the possible coding that the nervous system of toads uses for different prey stimuli, the neural mechanisms of habituation and dishabituation, and the dynamic changes that the command units may have during these processes. The model proposes specific hypothesis and experiments to clarify the nature of these processes and to test the validity of the command unit hypothesis.Research supported in part by CONACYT under grant PCCBBNA 021005Research supported in part by the NIH under grant NS 14971-05 from National Institute of Neurological and Communicative Disorders and Stroke     

Simulation of habituation to simple and multiple stimuli

Within the psychological literature there are a number of models that reproduce the defining properties of habituation to a single stimulus. However, most of them do not reproduce the phenomenon of dishabituation shown in empirical studies, consisting in the recovery of a stimulus previously habituated upon the appearance of a novel stimulus. The present work offers a model of habituation which, in addition to reproducing the basic properties of habituation to a stimulus, also does so when more than one stimulus is presented, and thus includes the dishabituation phenomenon. This model consists of two functions, one called "activation" and the other "availability", and is tested by means of simulation of the responses in the context of different stimulus patterns. The results of the simulation show a good qualitative fit to the empirical results on the phenomena of habituation, including dishabituation. In addition, the model is suitable for inclusion in associative models that reproduce classical conditioning, which will make it possible in the future to incorporate into these in a simple way the influence that the habituation of each stimulus may have on its association with other stimuli.     

Selectivity of visual cortical neurons of rabbits to magnitude of moving stimuli

Unit responses of the rabbit visual cortex were investigated in relation to size of visual stimuli moving in their receptive field. With an increase in size of the stimulus in a direction perpendicular to the direction of movement ("width" of the stimulus) an initial increase in the intensity of the unit response through spatial summation of excitory effects is followed by a decrease through lateral inhibition. This inhibition is observed between zones of the receptive field which behave as activating when tested by a stimulus of small size. Each neuron has its own "preferred" size of stimuli evoking its maximal activation. No direct correlation is found between the "preferred" stimulus size and the size of the receptive field. With a change in stimulus size in the direction of movement ("length" of the stimulus) the responses to stimuli of optimal size may be potentiated through mutual facilitation of the effects evoked by the leading and trailing edges of the stimulus and weakened in response to stimuli of large size. The selective behavior of the neurons with respect to stimulus size is intensified in the case of coordinated changes in their length and width. It is postulated that the series of neurons responding to stimuli of different "preferred" dimensions may constitute a system classifying stimuli by their size.A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 4, No. 6, pp. 636–644, November–December, 1972.     

Characterisation of columnar neurons and visual signal processing in the medulla of the locust optic lobe by system identification techniques

We describe visual responses of seventeen physiological classes of columnar neuron from the retina, lamina and medulla of the locust (Locusta migratoria) optic lobe. Many of these neurons were anatomically identified by neurobiotin injection. Characterisation of neuronal responses was made by moving and flash stimuli, and by two system identification techniques: 1. The first-order spatiotemporal kernel was estimated from response to a spatiotemporal white-noise stimulus; 2. A set of kernels to second order was derived by the maximal-length shift register (M-sequence) technique, describing the system response to a two-channel centre-surround stimulus. Most cells have small receptive fields, usually with a centre diameter of about 1.5°, which is similar to that of a single receptor in the compound eye. Linear response components show varying spatial and temporal tuning, although lateral inhibition is generally fairly weak. Second-order nonlinearities often have a simple form consistent with a static nonlinear transformation of the input from the large monopolar cells of the lamina followed by further linear filtering.Abbreviations LMC large monopolar cell - LVF long visual fibre - RF receptive field - SMC small monopolar cell - SVF short visual fibre     

Auditory pre-experience modulates classification of affect intensity: evidence for the evaluation of call salience by a non-human mammal,the bat <Emphasis Type="Italic">Megaderma lyra</Emphasis>

Introduction

Immediate responses towards emotional utterances in humans are determined by the acoustic structure and perceived relevance, i.e. salience, of the stimuli, and are controlled via a central feedback taking into account acoustic pre-experience. The present study explores whether the evaluation of stimulus salience in the acoustic communication of emotions is specifically human or has precursors in mammals. We created different pre-experiences by habituating bats (Megaderma lyra) to stimuli based on aggression, and response, calls from high or low intensity level agonistic interactions, respectively. Then we presented a test stimulus of opposite affect intensity of the same call type. We compared the modulation of response behaviour by affect intensity between the reciprocal experiments.

Results

For aggression call stimuli, the bats responded to the dishabituation stimuli independent of affect intensity, emphasising the attention-grabbing function of this call type. For response call stimuli, the bats responded to a high affect intensity test stimulus after experiencing stimuli of low affect intensity, but transferred habituation to a low affect intensity test stimulus after experiencing stimuli of high affect intensity. This transfer of habituation was not due to over-habituation as the bats responded to a frequency-shifted control stimulus. A direct comparison confirmed the asymmetric response behaviour in the reciprocal experiments.

Conclusions

Thus, the present study provides not only evidence for a discrimination of affect intensity, but also for an evaluation of stimulus salience, suggesting that basic assessment mechanisms involved in the perception of emotion are an ancestral trait in mammals.

     

Feedback control and quantification of the response of EEG alpha to visual stimulation

The response of the posterior EEG alpha rhythms to visual stimulation is so variable that it is difficult to obtain reliable on-line measurement of it. Feedback between the EEG alpha and the visual stimulus (1) reduces random variation in the response and (2) facilitates on-line quantification. With feedback EEG, the response to visual stimulation is measured as a series of time durations of alpha and of no-alpha intervals in the EEG. This time series occurs in two stages: an initial disturbance followed by a recovery. The quantification of the series of time durations is achieved by fitting curves to the series of alpha time intervals and of no-alpha time intervals. These functions, computed in each trial of 30 stimulations, are an objective, quantitative definition of EEG response. The utility of the method was demonstrated by testing it with reference to well-known effects. Habituation to a repeated stimulus, dishabituation, habituation to a class of stimuli, dishabituation by changing the class of stimuli, and differences among brain-lesioned, psychiatric patients and normals were shown with a detailed quantification. It was concluded that biofeedback is the method of choice for quantitative research on the EEG component of the human orienting response.     

Properties of neurons of the tectal portion of the visual system of the axolotl Ambystoma mexicanum]

In the tectum opticum of the adult neotenic A. mexicanum, responses of single neuronal units to diffuse illumination and moving visual stimuli have been investigated. Of 111 unites investigated, 27 are presented by tectal neurons, their maximum distribution being observed at a depth of 500-600 mu. In superficial layers 9 ipsi-elements were found; their receptive fields are located in the antero-dorsal part of the visual field, at both sides of the body axis. Among the units identified as the terminals of visual fibers, 70% have receptive fields of 5-10 degrees, being localized in general more close to the surface as compared to the units with the receptive field diameter of 40 and more degrees (11%). Visual neurons and ganglionic retinal cells with axons terminating in the tectum, exhibit poor specificity to the size of a stimulus within 5-30 degrees and do not react to stimuli of 2 degrees.     

Responses of mink to auditory stimuli: Prerequisites for applying the ‘cognitive bias’ approach

The aim of the study was to determine and validate prerequisites for applying a cognitive (judgement) bias approach to assessing welfare in farmed mink (Neovison vison). We investigated discrimination ability and associative learning ability using auditory cues. The mink (n = 15 females) were divided into two groups (High, n = 8; Low, n = 7, representing the frequency of the tone they were habituated to, 18 and 2 kHz respectively) and were tested using a habituation–dishabituation procedure in experiment 1. In experiment 2 one auditory stimulus was followed by an inter-trial-interval (safe/neutral situation), whereas another auditory stimulus was followed by an aversive stimulus (air blow) before the inter-trial-interval (danger situation). We observed behaviour including latencies to show a response during both experiments. The High mink showed significant habituation in experiment 1 but the Low mink only showed habituation in experiment 2. Regardless of the frequency used (2 and 18 kHz), cues predicting the danger situation initially elicited slower responses compared to those predicting the safe situation but quickly became faster. Using auditory cues as discrimination stimuli for female farmed mink in a judgement bias approach would thus appear to be feasible. However several specific issues are to be considered in order to successfully adapt a cognitive bias approach to mink, and these are discussed.     

Tectal responses to potassium loads and subsequent visual stimuli in the toad, Bufo bufo

Calling male toads were tested behaviourally for their prey catching responses to wormlike stimuli and assigned to groups of non-hungry and hungry depending on their prey catching motivation before being prepared for visual unit, massed unit and slow potential shift (SPS) recording from the optic tectum. Control recordings to visual stimuli were made before recording the effects of application of isotonic solutions containing concentrations of 0-41 mM K(+). Application of solution was followed by presentation of the visual stimulus while the solution still bathed the tectum. The best tectal responses were made to large square visual stimuli in the non-hungry toads, perhaps because recordings were made in the breeding season. Responses of the tectum to solution addition were significant in the concentration range of 7-17 mM K(+). Hungry toads showed an earlier, smaller response than non-hungry (sexually motivated) animals. When the visual stimulus was presented, there were unit and massed unit responses at all bathing solution concentrations, which were larger in non-hungry animals. These experiments revealed that toads motivated to feed respond earlier than non-hungry toads to application of artificial CSF to the tectum, though non-hungry toads responded best to the subsequent visual stimulus.     

Question of “head preference” in response to worm-like dummies during prey-capture of toads,Bufo bufo

If a black worm-like dummy is moving against a white background, toads fixate and snap at the leading end of the stimulus. This “head preference” phenomenon is — within limits — independent of (i) background structure, and (ii) stripe length. “Head preference” can be disturbed by reducing the amount of the stimulus background contrast as well as by point structures incorporated in the worm-like shape of the stimulus. If the stimulus-background contrast of the worm dummy is reversed, toads exhibit a clear preference in fixating and snapping for the trailing end of the stimulus. This “tail preference” is independent of changes in (i) and (ii). The neural basis of “head preference” or “tail preference” respectively, is discussed.     

Neurophysiological mechanisms underlying habituation of the tentacle retraction reflex in the land slug Ariolimax

Habituation of the tentacle retraction reflex was studied at the following response levels: (1) Muscle tension elicited in the tentacle retractor muscle by repeated stimulation of a cerebral nerve (at 60-sec intervals) declined in parallel with evoked activity of the largest unit in the tentacle retractor nerve. (2) The largest unit in the tentacle retractor nerve (L₄) showed spontaneous recovery and dishabituation. The rate of response decrement was inversely related to the strength of stimulus, and an optimal interstimulus interval ca. 60 s was found. Retention of habituation for 24 h was exhibited. (3) The major retractor motoneurons (L₂, L₃, L₄) all showed habituation, dishabituation, and spontaneous recovery. The decline of L₄ activity was parallelled by a decline in muscle response. (4) Compound EPSPs elicited in the retractor motoneurons by stimulation of sensory pathways showed habituation and dishabituation. (5) Unitary EPSPs elicited by stimulation of cerebral nerves and connectives with minimal stimulus strengths also showed habituation and were unaffected by spontaneously occurring EPSPs. Dishabituation by another pathway was also shown. (6) Depolarization of L₄ by a constant current produced spike trains of constant firing rate and evoked a constant level of muscle tension in repeated trials, suggesting the absence of habituation in a peripheral nerve net or at the neuromuscular junction.     

Vision and electroreception: Integration of sensory information in the optic tectum of the weakly electric fishApteronotus albifrons

Summary The responses of single neurons to visual and electrosensory stimulation were studied in the optic tectum of the weakly electric fishApteronotus albifrons. Most of the cells recorded in the region of the tectum studied, the anterior medial quadrant, were poorly responsive or completely insensitive to flashes of light or to bursts of AC electrical stimuli applied to the entire fish. However, these cells gave vigorous responses to moving visual or electrosensory stimuli. Most cells showed differences in their response contingent upon the direction of the stimulus movement and most received input from both the visual and electrosensory systems. Electrosensory responses to moving stimuli were depressed by jamming stimuli, 4 Hz amplitude modulation of the animal's electric organ discharge, presented simultaneously with the moving stimulus. However, the jamming signal presented alone typically evoked no response. Moving visual stimuli, presented simultaneously with the electrosensory, were usually able to restore the magnitude of a response toward its value in the unjammed situation. For most of the cells studied the receptive fields for vision and electroreception were in register. In some cases the visual and electrosensory components could be separated by presenting the two types of stimuli separately, or by presenting both simultaneously but with some amount of spatial separation, which causes the two to be misaligned relative to the fish. In other cases the individual responses could not be separated by spatial manipulations of the two stimuli and in these cases differences in the alignment of the two types of stimuli could cause changes in the intensity of the cells' responses.Abbreviations AM amplitude modulation - EOD electric organ discharge - PLLL posterior lateral line lobe     

Binocular depth perception mechanisms in tongue-projecting salamanders

Tongue-projecting salamanders (Bolitoglossini) combine extreme speed and high precision in prey capture. They possess all requirements for stereoscopic depth perception: frontally oriented eyes, a substantial amount of direct ipsilateral projection in addition to the contralateral one, and binocularly driven neurons. Extracellular recordings were made from retinal afferents in the tectum as well as from the somata of tectal neurons. RF-sizes of afferents and tectal neurons were determined, and the response properties of tectal neurons were tested under monocular and binocular conditions with stimuli of different size and velocity. While RF-sizes and response properties of binocular neurons during binocular and contralateral stimulation were similar, ipsilaterally stimulated neurons exhibited much smaller RFs, lower spike rates and different size preferences.Furthermore, the contralateral retinotectal projection from one eye and the ipsilateral from the other are in register. While retinal afferents are distributed linearly over the tectal surface, most tectal neurons are activated by a retinal area corresponding to the frontal visual field; this results in a magnification of this region. The two monocular receptive fields of binocular neurons exhibit zero disparities (horopter) at distances that coincide with the maximum reach of the tongue. We hypothesize that bolitoglossine salamanders (as well as amphibians in general) make use of two kinds of disparities: (1) between the maps in the left and right tectal hemisphere, coding for the lateral eccentricity of an object, and (2) between the ipsilateral and contralateral retinotectal map, coding for the distance. The presence of substantial direct ipsilateral afferents in bolitoglossine salamanders appears to be the basis for a fast computation of object distance, which is characteristic of these animals.Abbreviations Ax/Ay coordinates of a recorded afference - Nx/Ny coordinates of a recorded neuron - RF receptive field - RFc contralateral receptive field - RFi ipsilateral receptive field - RFx/RFy coordinates of a receptive field center - RGC retinal ganglion cell     

The synaptic origins of receptive field properties in the cricket cercal sensory system

Summary The regional distribution of cerebral glucose utilization, revealed by the¹⁴C-2DG technique, was compared between (i) toads after stimulus-specific long-term habituation of the orienting response toward a repeatedly presented prey dummy (habituation group) and (ii) non-habituated toads, readily orienting toward the repetitively presented prey stimulus (naive group). In the habituation group, the ventral medial pallium (vMP), a certain portion of the preoptic area (PO), and the dorsal hypothalamus (dHYP) showed a statistically significantincrease in¹⁴C-2DG-uptake;decrease was observed in the ventral layers of the optic tectum (vOT), a portion of the tegmental reticular formation (RET), the ventral cerebellum (vCB), and the striatum (STR). The results suggest that stimulus-specific long-term habituation of prey-catching affects both, components of thestimulus-response mediating circuit (e.g., involving OT), and structures extrinsic to it, (e.g., vMP, PO, dHYP), which may belong to amodulatory circuitry. Bilateral lesions to vMP strongly delay habituation. Our results are suggesting that damping of the adequate behavioral motor response during habituation involves active inhibitory processes of a modulatory system that develops in strength during stimulus repetition so as to suppress response output, which basically supports Sokolov's hypothesis (1975).Abbreviations A anterior dorsal thalamic nucleus - AL amygdala, lateral portion - dCB dorsal half of the cerebellum - vCB ventral half of the cerebellum - DP dorsal pallium - dHYP dorsal hypothalamus - pLP posterior half of the lateral pallium - Lpd lateral postero-dorsal thalamus - Lpv lateral postero-ventral thalamus - aMP anterior third of the medial pallium - dMP dorsal portion of the posterior medial pallium - vMP ventral two-third of the posterior medial pallium - MS medial septum - dOT dorsal layers of the optic tectum - vOT ventral layers of the optic tectum - P posterior thalamic nucleus - PO preoptic area - RET tegmental portion of the medial reticular formation - STR striatum, dorsal and ventral portion - vTEG ventral tegmentum