Bernhard Ronacher

Desert ants Cataglyphis fortis use self-induced optic flow to measure distances travelled

While foraging, desert ants of the genus Cataglyphis use a vector navigation (route integration) system for homing. Any vector navigation system requires that the animal is able to evaluate the angles steered and the distances travelled. Here we investigate whether the ants acquire the latter information by monitoring self-induced optic flow. To answer this question, the animals were trained and tested within perspex channels in which patterns were presented underneath a transparent walking platform. The patterns could be moved at different velocities (up to > 0.5 the ants walking speed) in the same or in the opposite direction relative to the direction in which the animal walked. Experimental manipulations of the optic flow influenced the ants homing distances (Figs. 2 and 4). Distance estimation depends on the speed of self-induced image motion rather than on the contrast frequency, indicating that the motion sensitive mechanism involved is different from mechanisms mediating the optomotor response. Experiments in which the ants walked on a featureless floor, or in which they wore eye covers (Fig. 6), show that they are able also to use additional (probably kinesthetic) cues for assessing their travel distance. Hence, even though optic flow cues are not the only ones used by the ants, the experiments show that ants are obviously able to exploit such cues for estimation of travel distance.

Filtering of behaviourally relevant temporal parameters of a grasshopper's song by an auditory interneuron

SummaryIn females of the acridid grasshopperChorthippus biguttulus, thoracic auditory interneurons were investigated with respect to their selectivity for temporal parameters of the conspecific song. Special attention was given to the detection of small gaps in the ‘syllables’ of the song, since behavioural experiments have shown that the presence or absence of gaps is critical for the females Innate Releasing Mechanism (cf. Fig. 1).The spiking response of one ascending interneuron, the AN4, shows filtering properties which closely resemble the behavioural reactions (cf. Figs. 1, 3 and 5b). The difference in the AN4s reaction to stimuli with gaps and uninterrupted stimuli is maintained over the behaviourally relevant intensity range (Fig. 4). This reaction is reliable enough that the stimulus type could be inferred by higher centres even from single stimulus presentations. Hence, this neuron is likely to participate in the task of gap detection and probably is a part of the neuronal filter network which determines the characteristics of the Innate Releasing Mechanism of this species. However, this interneuron is not species-specific: A homologue exists in other acridids as well and, inLocusta migratoria, has similar response characteristics (Fig. 6). The inferences of this observation for the evolution of an Innate Releasing Mechanism are discussed.

Routes and stations in the processing of auditory directional information in the CNS of a grasshopper, as revealed by surgical experiments

SummaryMale grasshoppers of the acridid speciesChorthippus biguttulus respond to conspecific female song by turning abruptly toward the sound source and then singing themselves. The orienting response requires that (i) the male recognizes the female song and (ii) determines the location of its source. By observing the effects of various forms of surgical interference (cutting connectives, splitting ganglia, destruction of a tympanal organ) on the subsequent behavior, we were able to narrow down the paths of information flow necessary for these abilities and to make an estimate of the contributions of individual ganglia to the evaluation of sound direction.1.The information from a single tympanal organ is sufficient for therecognition of the conspecific song. From the metathoracic ganglion (TG3) sufficient information for song recognition ascends both in the ipsilateral and in the contralateral connective chain. Thus, information for song recognition is transmitted to the opposite side within the metathoracic ganglion.2.For a singing response to be elicited by hearing a female chirp, it is necessary and sufficient that the connectives linking TG3 and the supraesophageal ganglion (brain) of the male be intact on at least one side (as has been shown forGomphocerippus rufus by Loher and Huber 1966, and Elsner and Huber 1969). Neither the three thoracic ganglia alone nor the thoracic-ganglion complex plus the subesophageal ganglion suffice to elicit either the turning or the singing response. The most probable explanation of our results is that the information paths for both responses make a loop via the brain.3.A crucial step in sound direction processing takes place within TG3 itself. The results after connective cutting indicate a reciprocally inhibitory interaction within this ganglion by which the difference between right and left tympanal input is enhanced.4.The information about sound direction carried in either connective alone is incomplete. Therefore, an additional ‘comparator element’ must exist, which receives the ‘directional signals’ from both connectives and converts them into an unambiguous turning command. This step in direction processing must occur either in the brain or along the pathways descending from the brain to the anterior two thoracic ganglia.5.The anterior two thoracic ganglia, as well as the subesophageal ganglion, make either no contribution or a negligibly small contribution to the determination of sound direction.

Spike synchronization of tympanic receptor fibres in a grasshopper (Chorthippus biguttulus L., Acrididae): a possible mechanism for detection of short gaps in model songs

Summary1.In recordings from single tympanic receptor fibres inC. biguttulus, the response to synthesized sounds (rectangularly modulated white noise) interrupted by very brief (a few milliseconds) gaps was examined. In behavioral tests, females of the species respond very differently to such ‘model syllables’ at moderate intensities, depending on the gap width. If the gaps (in a moderateintensity syllable) are larger than 2 ms, the stimulus fails to elicit a response, whereas stimuli with gaps smaller than 1 ms are as effective as uninterrupted yllables (D. von Helversen 1972; O. von Helversen 1979).2.Neither the mean spike count nor the interspike-interval distribution of the single receptor response contains the information sufficient to distinguish uninterrupted syllables from syllables with gaps (Figs. 2 and 3). On the other hand, examination of the temporal distribution of the spikes reveals that gaps (or the pulse onsets following the gaps) cause spike synchronization (Fig. 4).3.An index of synchronization (IS) was defined as a measure of this gap-induced effect (Figs. 5 and 6). Analysis of the receptor responses based on IS revealed differences that correspond quantitatively to the abrupt abolition of the behavioral response at a gap-width between 1 and 2 ms. From the hypothesis that such brief gaps are detected by the nervous system by way of spike synchronization in the tympanic nerve, one can predict certain features of the behavioral response to highintensity stimuli.4.The gap-induced spike synchronization was more pronounced at higher temperatures. This effect was demonstrated in both summated recordings from the tympanic nerve and single fibre recordings (Fig. 8).5.Experiments with primary auditory fibres ofLocusta migratoria showed that the receptors in this species respond very similarly to the same stimuli. That is, the receptors ofC. biguttulus are not specially adapted for detecting very brief gaps. Synchronization of the spikes in parallel receptor fibres of the tympanal nerve is probably a general feature of acridids; we infer that inC. biguttulus this gap-induced synchronized activity is detected by special processing in higher auditory centres.

Stridulation of acridid grasshoppers after hemisection of thoracic ganglia: evidence for hemiganglionic oscillators

SummaryIn the grasshopperChorthippus biguttulus the stridulatory movements of males with surgically manipulated ventral nerve cords were investigated.1.The stridulation pattern of animals with a hemisected mesothoracic ganglion was indistinguishable from that of intact animals.2.After hemisection of the metathoracic ganglion several animals were still able to stridulate in the species-specific pattern (Figs. 3, 5). Different structural elements of the song, however, were affected to different degrees by this operation. Although the stereotyped up-and-down movements were normal, the rhythm of pauses, which in intact animals are inserted after every third to fourth up- and-down cycle, was disturbed. As a result, the variation of syllable lengths was much higher (Fig. 4).3.A prominent feature after hemisection of the metathoracic ganglion was an almost complete loss of coordination between left and right hind legs (Figs. 5–7). Only in the coarse structure of the song (e.g. the beginning and termination of song sequences) was a correlation of the leg movements still discernible. This was especially obvious in songs of the rivalry type and in precopulatory kicking movements (Fig. 8).4.If in addition to hemisection of the metathoracic ganglion one of the neck connectives was transected the animals stridulated only with the hind leg ipsilateral to the intact connective (Fig. 11).5.Even after hemisection of both the meso- and metathoracic ganglia, animals were able to produce the species-specific stridulation pattern (Fig. 9).6.In animals with hemisected metathoracic ganglia and both connectives between pro- and mesothoracic ganglia transected, components of the species-specific pattern could be induced by current injection into the mesothoracic ganglion (Fig. 10).7.These results suggest that the stridulation rhythm-producing neuronal network is composed of hemisegmental subunits. A hemiganglionic structure of rhythm generators might reflect the ancestral organization of locomotion-controlling networks.

Perception of electric properties of objects in electrolocating weakly electric fish: two-dimensional similarity scaling reveals a City-Block metric

During electrolocation weakly electric fish monitor their self-emitted electric signals in order to detect and evaluate nearby objects. Individuals of the mormyrid species Gnathonemus petersii were trained to discriminate between resistive and capacitive objects that differed only in their electric properties. Capacitive properties are found almost exclusively among living objects, and are thus of special importance to the fish. Resistive and capacitive properties of objects influence the amplitude and waveform of the perceived electrolocation signals in different ways. Resistive objects change only signal amplitude, whereas capacitive objects affect both amplitude and waveform. The electro-perceptual system of weakly electric fish was investigated by systematic variation of amplitude and waveform using objects of various electric properties as electrolocation targets. After training with a particular stimulus set, the fish reacted in a graded manner to differences in both signal parameters. The perception of each stimulus dimension was found to be independent of the other one. In a kind of ‘cross modality matching’ experiment, amplitude and waveform parameters were tested against one another. For each amplitude value there was a corresponding waveform value that was judged by the fish to be equally different from the training stimuli. Because of these results, a two-dimensional “perceptual space” is postulated with the two stimulus dimensions waveform and amplitude as its axes. A scaling procedure, using Minkowski metrics, was applied to determine the fishs “perceptual metric”. The City-Block metric, and not the Euclidean metric, provided the best description of the data. The two signal dimensions were found to be separable, i.e. to combine additively in complex stimuli. The results are discussed with regard to the discrimination of animate and inanimate objects in the natural environment of the fish.

Efficient transformation of an auditory population code in a small sensory system

Optimal coding principles are implemented in many large sensory systems. They include the systematic transformation of external stimuli into a sparse and decorrelated neuronal representation, enabling a flexible readout of stimulus properties. Are these principles also applicable to size-constrained systems, which have to rely on a limited number of neurons and may only have to fulfill specific and restricted tasks? We studied this question in an insect system—the early auditory pathway of grasshoppers. Grasshoppers use genetically fixed songs to recognize mates. The first steps of neural processing of songs take place in a small three-layer feed-forward network comprising only a few dozen neurons. We analyzed the transformation of the neural code within this network. Indeed, grasshoppers create a decorrelated and sparse representation, in accordance with optimal coding theory. Whereas the neuronal input layer is best read out as a summed population, a labeled-line population code for temporal features of the song is established after only two processing steps. At this stage, information about song identity is maximal for a population decoder that preserves neuronal identity. We conclude that optimal coding principles do apply to the early auditory system of the grasshopper, despite its size constraints. The inputs, however, are not encoded in a systematic, map-like fashion as in many larger sensory systems. Already at its periphery, part of the grasshopper auditory system seems to focus on behaviorally relevant features, and is in this property more reminiscent of higher sensory areas in vertebrates.

Evolutionarily conserved coding properties of auditory neurons across grasshopper species

We investigated encoding properties of identified auditory interneurons in two not closely related grasshopper species (Acrididae). The neurons can be homologized on the basis of their similar morphologies and physiologies. As test stimuli, we used the species-specific stridulation signals of Chorthippus biguttulus, which evidently are not relevant for the other species, Locusta migratoria. We recorded spike trains produced in response to these signals from several neuron types at the first levels of the auditory pathway in both species. Using a spike train metric to quantify differences between neuronal responses, we found a high similarity in the responses of homologous neurons: interspecific differences between the responses of homologous neurons in the two species were not significantly larger than intraspecific differences (between several specimens of a neuron in one species). These results suggest that the elements of the thoracic auditory pathway have been strongly conserved during the evolutionary divergence of these species. According to the ‘efficient coding’ hypothesis, an adaptation of the thoracic auditory pathway to the specific needs of acoustic communication could be expected. We conclude that there must have been stabilizing selective forces at work that conserved coding characteristics and prevented such an adaptation.

Nonlinear Computations Underlying Temporal and Population Sparseness in the Auditory System of the Grasshopper

Sparse coding schemes are employed by many sensory systems and implement efficient coding principles. Yet, the computations yielding sparse representations are often only partly understood. The early auditory system of the grasshopper produces a temporally and population-sparse representation of natural communication signals. To reveal the computations generating such a code, we estimated 1D and 2D linear-nonlinear models. We then used these models to examine the contribution of different model components to response sparseness. 2D models were better able to reproduce the sparseness measured in the system: while 1D models only captured 55% of the population sparseness at the networks output, 2D models accounted for 88% of it. Looking at the model structure, we could identify two types of computation, which increase sparseness. First, a sensitivity to the derivative of the stimulus and, second, the combination of a fast, excitatory and a slow, suppressive feature. Both were implemented in different classes of cells and increased the specificity and diversity of responses. The two types produced more transient responses and thereby amplified temporal sparseness. Additionally, the second type of computation contributed to population sparseness by increasing the diversity of feature selectivity through a wide range of delays between an excitatory and a suppressive feature. Both kinds of computation can be implemented through spike-frequency adaptation or slow inhibition—mechanisms found in many systems. Our results from the auditory system of the grasshopper are thus likely to reflect general principles underlying the emergence of sparse representations.

HOW DO BEES LEARN AND RECOGNIZE VISUAL PATTERNS

Abstract. The basic task of perceptual systems is the recognition and localization of objects. The central nervous system has to solve these problems on the basis of the excitation patterns of sensory nerves, in spite of the fact that these provide only ambiguous information about objects. Two processing principles seem to be fundamental for an efficient formation of object representations: the extraction of characteristic features and the ability to assess similarities between different objects. This article reviews investigations in which different training paradigms were applied in order to explore the honeybees capacities to learn and recognize visual patterns. One aim of these experiments is to assess whether insects use similar processing mechanisms as vertebrates, for instance human beings. By comparing the computational performance of perceptual systems in animals with different evolutionary history we can hope to learn more about the operation of basic rules in nervous systems.“The messages which the brain receives have not the least similarity with the stimuli. They consist in pulses of given intensities and frequencies, characteristic for the transmitting nerve-fiber, which ends at a definite place of the cortex. ... From this information it produces the image of the world by a process which can metaphorically be called a consummate piece of combinatorial mathematics: it sorts out of the maze of indifferent and varying signals, invariant shapes and relations which form the world of ordinary experience.” Max Born (1949)