Efficiency and the role of adaptation in klinokinesis

Klinokinesis is a behavioral mechanism in which an organism moves toward or away from a stimulus source by altering its frequency of change of direction without biasing its turns with respect to the stimulus field. Computer simulation was used to study the efficiency of, and the effect of sensory adaptation on, this behavioral strategy. In modeling an organism with perfect performance (no error in determining the intensity of the stimulus and ability to move in perfectly straight lines) efficiency was about 70% without adaptation, and declined as the rate of adaptation increased. In contrast, models with non-perfect (noisy) performance were frequently able to double or triple their reduced efficiency by adapting to the stimulus intensity. Three types of noise that degraded performance were simulated: (1) intensity noise described random fluctuations in the intensity of the stimulus that were not associated with movement of the organism in the stimulus field; (2) motor noise described random fluctuations in the direction of locomotion as the organism moved along; (3) developmental noise described random differences between individuals in a constant tendency to turn to a certain degree as they moved forward. Adaptation had similar effects with any of the three types of noise. If a particular type of noise was strong enough to degrade performance significantly, then optimal performance occurred with an adaptation rate of about 0.2 per step.     

Behavioral Responses of Meloidogyne incognita to Small Temperature Changes

Small, rapid temperature changes were generated by incandescent radiation, and behavioral responses of Meloidogyne incognita juveniles were recorded with high time resolution by computer tracking. Temperature changes away from the preferred temperature resulted in decreases in the rate of movement and increases in the rate of change of direction, whether the changes were toward warmer or cooler temperatures. These behavioral changes lasted about 30 seconds. Temperature changes toward the preferred temperature caused the response rates to change in the opposite directions, and the behavioral changes persisted for several minutes. These results demonstrate that nematodes can respond to a purely temporal thermal stimulus in a manner consistent with efficient indirect orientation or klinokinesis. The rate of temperature change was estimated to be of the order of 10⁻⁴ C/second, suggesting that the nematodes detected a change of about 0.001 C.     

Influence of sound pressure level on the processing of amplitude modulations by auditory neurons of the locust

Typical features of natural sounds are amplitude changes at different time scales. In many species, amplitude modulations constitute decisive cues to recognize communication signals. Since these signals should be recognizable over a broad intensity range, we investigated how the encoding of amplitude modulations by auditory neurons depends on sound pressure level. Identified neurons that represent different processing stages in the locusts’ auditory pathway were stimulated with sinusoidal modulations of a broad band noise carrier, at different intensities, and characteristic parameters of modulation transfer functions (MTFs) were determined. The corner frequencies of temporal MTFs turned out to be independent of intensity for all neurons except one. Furthermore, for none of the neurons investigated corner frequencies were significantly correlated with spike rate, indicating a remarkable intensity invariance of the upper limits of temporal resolution. The shape of the tMTFs changed with increasing intensity from a low-pass to a band-pass for receptors and local neurons, while no consistent change was observed for ascending neurons. The best modulation frequency depended on intensity and spike rate, especially for receptors and local neurons. Remarkably, the adaptation state of some neurons turned out to be independent of the spike rate during the modulation part of the stimulus.     

Electrical studies on the compound eye of Ligia occidentalis Dana (Crustacea: Isopoda)

The ERG of the compound eye in freshly collected Ligia occidentalis, in response to high intensity light flashes of ⅛ second or longer duration, begins with a negative on-effect quickly followed by an early positive deflection, rapidly returns to the baseline during illumination, and ends with a positive off-effect. As the stimulus intensity is decreased the early positivity progressively decreases and the rapid return to the baseline is replaced by a slowing decline of the negative on-effect. Responses were recorded with one active electrode subcorneally situated in the illuminated eye, the reference electrode in the dark eye. The dark-adapted eye shows a facilitation of the amplitude and rates of rise and fall of the on-effect to a brief, high intensity light stimulus. This facilitation may persist for more than 2 minutes. Following light adaptation under conditions in which the human eye loses sensitivity by a factor of almost 40,000 the Ligia eye loses sensitivity by a factor of only 3. The flicker fusion frequency of the ERG may be as high as 120/second with a corneal illumination of 15,000 foot-candles. Bleeding an otherwise intact animal very rapidly results in a decline of amplitude, change of wave form, and loss of facilitation in the ERG. When the eye is deganglionated without bleeding the animal the isolated retina responds in the same manner as the intact eye. Histological examination of the Ligia receptor layer showed that each ommatidium contains three different retinula cell types, each of which may be responsible for a different aspect of the ERG.     

Differential production of chirping behavior evoked by electrical stimulation of the weakly electric fish, Apteronotus leptorhynchus

Aperonotus leptorhynchus (Gymnotiformes) produces wave-like electric organ discharges distinguished by a high degree of constancy. Transient frequency and amplitude modulations of these discharges occur both spontaneously and during social interactions, which can be mimicked by external electrical stimulation. The so-called chirps can be divided into four different types. Independent of the type of chirp produced under spontaneous conditions, the fish generate only significant numbers of type-2 chirps under evoked conditions. The rate of production of chirps of this type is largely determined by the frequency relative to the fish's frequency and signal intensity. Frequencies of + 10 Hz of the fish's own discharge frequency most effectively elicit chirps. Type-2 chirps can also be evoked through stimulation at or near the higher harmonic frequencies of the fish's frequency, but the chirp rate decreases with increasing number of the higher harmonic component. Over a certain range, the rate of production of type-2 chirps increases with increasing stimulus intensity. At very high intensities the generation of type-2 chirps is accompanied by the production of a novel type of electrical signal ("abrupt frequency rise") characterized by a frequency increase of approximately 20 Hz and high repetition rates of roughly 10 s(-1). We hypothesize that the different types of electric modulations subserve different behavioral functions.     

Adapting-bump model for eccentric cells of Limulus

Light-evoked intracellular voltage noise records have been obtained from Limulus eccentric cells, from threshold light intensity to an intensity .10(5) times threshold. These data are analyzed in terms of a simple "adapting-bump" noise model. It is shown how the model yields a data reduction procedure that slightly generalizes the familiar use of Campbell's theorem for Poisson shot noise: the correlative effect of adaptation amends Campbell's theorem by a single multiplicative factor, which may be estimated directly from the power spectrum of the noise data. The model also permits direct estimation of the bump shape from the power spectrum. The bump shape estimated from noise at dim light is in excellent agreement with the average shape of bumps observed directly in the dark. The data yield a bump rate that is linear with light up through about 50 times threshold intensity but that falls short of linearity by a factor of 35 at the brightest light. The bump height decreases as the -0.4 power of light intensity across the entire range. Bump duration decreases by a factor of 2 across the entire range, and the adaptation correlation factor descends from unity to about one-third. The modest change of the adaptation correlation shows that naive application of Campbell's theorem to such data is adequate for rough estimation of the model's physiological parameters. This simple accounting for all the data gives support to the adapting-bump model.     

Encoding repetition rate and duration in the inferior colliculus of the big brown bat,Eptesicus fuscus

1. Encoding of temporal stimulus parameters by inferior collicular (IC) neurons of Eptesicus fuscus was studied by recording their responses to a wide range of repetition rates (RRs) and durations at several stimulus intensities under free field stimulus conditions. 2. The response properties of 424 IC neurons recorded were similar to those reported in previous studies of this species. 3. IC neurons were classified as low-pass, band-pass, and high-pass according to their preference for RRs and/or durations characteristic of, respectively, search, approach, or terminal phases of echolocation. These neurons selectively process stimuli characteristic of the various phases of hunting. 4. Best RRs and best durations were not correlated with either the BFs or recording depths This suggests that each isofrequency lamina is capable of processing RRs and durations of all hunting phases. 5. Responses of one half of IC neurons studied were correlated with the stimulus duty cycle. These neurons may preferentially process terminal phase information when the bat's pulse emission duty cycle increases. 6. While the stimulus RR affected the dynamic range and overall profile of the intensity rate function, only little effect was observed with different stimulus durations.     

Adaptation to stimulus contrast and correlations during natural visual stimulation

In this study, we characterize the adaptation of neurons in the cat lateral geniculate nucleus to changes in stimulus contrast and correlations. By comparing responses to high- and low-contrast natural scene movie and white noise stimuli, we show that an increase in contrast or correlations results in receptive fields with faster temporal dynamics and stronger antagonistic surrounds, as well as decreases in gain and selectivity. We also observe contrast- and correlation-induced changes in the reliability and sparseness of neural responses. We find that reliability is determined primarily by processing in the receptive field (the effective contrast of the stimulus), while sparseness is determined by the interactions between several functional properties. These results reveal a number of adaptive phenomena and suggest that adaptation to stimulus contrast and correlations may play an important role in visual coding in a dynamic natural environment.     

Intensity Characteristics of the Noctuid Acoustic Receptor

Spiking activity of the more sensitive acoustic receptor is described as a function of stimulus intensity. The form of the intensity characteristic depends strongly on stimulus duration. For very brief stimuli, the integral of stimulus power over stimulus duration determines the effectiveness. No response saturation is observed. With longer stimuli (50 msec), a steady firing rate is elicited. The response extends from the spontaneous rate of 20–40 spikes/sec to a saturated firing rate of nearly 700 spikes/sec. The characteristic is monotonic over more than 50 db in stimulus intensity. With very long stimuli (10 sec), the characteristics are nonmonotonic. Firing rates late in the stimulus decrease in response to an increase in stimulus intensity. The non-monotonic characteristics are attributed to intensity-related changes in response adaptation.     

Adapting bump model for ventral photoreceptors of Limulus

Light-evoked current fluctuations have been recorded from ventral photoreceptors of Limulus for light intensity from threshold up to 10(5) times threshold. These data are analyzed in terms of the adapting bump noise model, which postulates that (a) the response to light is a summation of bumps; and (b) the average size of bump decreases with light intensity, and this is the major mechanism of light adaptation. It is shown here that this model can account for the data well. Furthermore, the model provides a convenient framework to characterize, in terms of bump parameters, the effects of calcium ions, which are known to affect photoreceptor functions. From responses to very dim light, it is found that the average impulse response (average of a large number of responses to dim flashes) can be predicted from knowledge of both the noise characteristics under steady light and the dispersion of latencies of individual bumps. Over the range of light intensities studied, it is shown that (a) the bump rate increases in strict proportionality to light intensity, up to approximately 10(5) bumps per second; and (b) the bump height decreases approximately as the -0.7 power of light intensity; at rates greater than 10(5) bumps per second, the conductance change associated with the single bump seems to reach a minimum value of approximately 10(-11) reciprocal ohms; (c) from the lowest to the highest light intensity, the bump duration decreases approximately by a factor of 2, and the time scale of the dispersion of latencies of individual bumps decreases approximately by a factor of 3; (d) removal of calcium ions from the bath lengthens the latency process and causes an increase in bump height but appears to have no effect on either the bump rate or the bump duration.     

Song switching and agonistic stimulation in the song sparrow (Melospiza melodia): five tests

Male song sparrows in southeastern Ontario have repertoires of five to 11 distinct song types. The singer repeats each song type a variable number of times before switching to another type. Analysis of territorial singing suggested that rate of switching song types is positively correlated with intensity of agonistic stimulation, where ‘agonistic’ signifies conflict-related. The song-switching hypothesis was tested with playback experiments which varied stimulus intensity in five different ways: (1) presence or absence of song stimuli; (2) addition of visual to auditory stimuli; (3) location of the song stimulus 20 m inside or outside territory; (4) nesting phases of the subjects; and (5) switching rate and rate of novel song type production of the playback (i.e. stimulus versatility). The subjects' switching rates and flight rates consistently increased with greater stimulation, although song rate tended to remain unaffected. The signalling of response intensity through adjustments in switching rate exemplifies how song repertoires function in agonistic communication.     

Influence of haptic guidance in learning a novel visuomotor task

In (re)learning of movements, haptic guidance can be used to direct the needed adaptations in motor control. Haptic guidance influences the main driving factors of motor adaptation, execution error, and control effort in different ways. Human-control effort is dissipated in the interactions that occur during haptic guidance. Minimizing the control effort would reduce the interaction forces and result in adaptation. However, guidance also decreases the magnitude of the execution errors, which could inhibit motor adaptation. The aim of this study was to assess how different types of haptic guidance affect kinematic adaptation in a novel visuomotor task. Five groups of subjects adapted to a reaching task in which the visual representation of the hand was rotated 30°. Each group was guided by a different force field. The force fields differed in magnitude and direction in order to discern the adaptation based on execution errors and control effort. The results demonstrated that the execution error did indeed play a key role in adaptation. The more the guiding forces restricted the occurrence of execution errors, the smaller the amount and rate of adaptation. However, the force field that enlarged the execution errors did not result in an increased rate of adaptation. The presence of a small amount of adaptation in the groups who did not experience execution errors during training suggested that adaptation could be driven on a much slower rate and on the basis of minimization of control effort as was evidenced by a gradual decrease of the interaction forces during training. Remarkably, also in the group in which the subjects were passive and completely guided, a small but significant adaptation occurred. The conclusion is that both minimization of execution errors and control effort drives kinematic adaptation in a novel visuomotor task, but the latter at a much slower rate.     

Male Calling Behavior and Female Choice in the Neotropical Treefrog Hyla microcephala

The effect of stimulus call complexity and calling rate on the vocal responses of males and female mate choice was studied in Hyla microcephala in Panama. Males increased the number of notes in their calls in response to increases in stimulus call complexity during both playback of 1 to 8-note advertisement calls and during natural interactions. However, precise matching of the number of notes in stimuli and responses did not occur consistently. Males also increased calling rates if stimuli were presented above prestimulus rates. Two-stimulus choice experiments demonstrated that females prefer both higher calling rates and greater call complexity, indicating that the ways males change their vocal behavior during interactions increases their attractiveness to potential mates. Tests in which the relative intensity of a high and low rate stimulus was varied indicated that females prefer stimuli with higher total sound energy. In a natural chorus, it is likely that females simply approach males giving the most conspicuous calls.     

Stochastic thermodynamic limit on E. coli adaptation by information geometric approach

Biological systems process information under noisy environment. Sensory adaptation model of E. coli is suitable for investigation because of its simplicity. To understand the adaptation processing quantitatively, stochastic thermodynamic approach has been attempted. Information processing can be assumed as state transition of a system that consists of signal transduction molecules using thermodynamic approach, and efficiency can be measured as thermodynamic cost. Recently, using information geometry and stochastic thermodynamics, a relationship between speed of the transition and the thermodynamic cost has been investigated for a chemical reaction model. Here, we introduce this approach to sensory adaptation model of E. coli, and examined a relationship between adaptation speed and the thermodynamic cost, and efficiency of the adaptation speed. For increasing external noise level in stimulation, the efficiency decreased, but the efficiency was highly robust to external stimulation strength. Moreover, we demonstrated that there is the best noise to achieve the adaptation in the aspect of thermodynamic efficiency. Our quantification method provides a framework to understand the adaptation speed and the thermodynamic cost for various biological systems.     

Analog modelling of cochlear adaptation

Adaptation phenomena in the peripheral hearing organ originate from the properties of the haircell-neuron synaps as revealed by their temperature dependency. In order to verify this hypothesis a model experiment is set up. The model consists of programming on an analog computer the equations describing the reaction kinetics from the frogs myoneural junction. A model neuron is attached to the synapsmodel in which two independent noise sources are incorporated. This noise addition serves to simulate the stochastic behavior of the transmitter release in the synaps resulting in a fluctuating generator potential and independently thereof to reflect the varying threshold of the nerve fiber. The reaction rate constants in the synaptic model were modified with respect to the original ones in order to get a coincidence of in vivo- and model results. The compound model primarily is used to simulate the quite different synchronization between the auditory nerve fibers occurring during intensity changes and during changes of the stimulus repetition rate. These results were known to be different in the animal experiments and were also generated by the model. It is shown clearly that neither synaptic noise alone nor membrane noise alone can account for the observations made in the animal experiments. Therefore a combination of both types of noise is used in this model. The model experiment also visualizes that amplitude changes for compound AP's during adaptation can be explained in toto by a decreasing synchronization, i.e. the broadening of the latency distribution function for the nerve fibers.     

Constructing Noise-Invariant Representations of Sound in the Auditory Pathway

Identifying behaviorally relevant sounds in the presence of background noise is one of the most important and poorly understood challenges faced by the auditory system. An elegant solution to this problem would be for the auditory system to represent sounds in a noise-invariant fashion. Since a major effect of background noise is to alter the statistics of the sounds reaching the ear, noise-invariant representations could be promoted by neurons adapting to stimulus statistics. Here we investigated the extent of neuronal adaptation to the mean and contrast of auditory stimulation as one ascends the auditory pathway. We measured these forms of adaptation by presenting complex synthetic and natural sounds, recording neuronal responses in the inferior colliculus and primary fields of the auditory cortex of anaesthetized ferrets, and comparing these responses with a sophisticated model of the auditory nerve. We find that the strength of both forms of adaptation increases as one ascends the auditory pathway. To investigate whether this adaptation to stimulus statistics contributes to the construction of noise-invariant sound representations, we also presented complex, natural sounds embedded in stationary noise, and used a decoding approach to assess the noise tolerance of the neuronal population code. We find that the code for complex sounds in the periphery is affected more by the addition of noise than the cortical code. We also find that noise tolerance is correlated with adaptation to stimulus statistics, so that populations that show the strongest adaptation to stimulus statistics are also the most noise-tolerant. This suggests that the increase in adaptation to sound statistics from auditory nerve to midbrain to cortex is an important stage in the construction of noise-invariant sound representations in the higher auditory brain.     

GABAergic inhibition shapes temporal and spatial response properties of pyramidal cells in the electrosensory lateral line lobe of gymnotiform fish

1. The amplitude-coding pyramidal neurons of the first-order nucleus in weakly electric gymnotiform fish (Eigenmannia), the electrosensory lateral line lobe (ELL), exhibit 2 major physiological transformations of primary afferent input. Pyramidal cells rapidly adapt to a step change in amplitude, and they have a center/surround receptive-field organization. This study examined the physiological role of GABAergic inhibition on pyramidal cells. GABAergic synapses onto the somata of pyramidal cells primarily originate from granule-cell interneurons along with descending input. 2. Pyramidal cells fall into two physiologically distinct categories: E units, which are excited by a rise in stimulus amplitude, and I units, which are inhibited by a rise in stimulus amplitude. Microiontophoretic application of bicuculline methiodide onto both types of pyramidal cells increased the time constant of adaptation, defined as the time required for the neuron's response to decay to 37% of its maximum value, by 70-90%. The peak firing rate of E units to a step increase in stimulus amplitude increased by 49%, while the firing rate of I units did not change significantly. 3. Bicuculline application demonstrated that GABAergic inhibition may contribute to the strict segregation of E and I response properties. In the presence of bicuculline, many E units (normally excited only by stimulus amplitude increases) became excited by both increases and decreases; many I units (normally excited only by amplitude decreases) also became excited to increases. 4. The size of the excitatory receptive-field of E units was not affected by bicuculline, although response magnitude increased. The inhibitory surround increased in spatial extent by 175% with bicuculline administration. Neither the size of the I unit receptive-field center nor the response magnitude changed in the presence of bicuculline. The antagonistic surround of I units, however, increased by 49%. 5. The anatomy of the ELL is well understood (see Carr and Maler 1986). The physiological results obtained in this study, along with the results of Bastian (1986a, b), further our understanding of the functional role of the ELL circuitry. Our results suggest that spatial and temporal response properties of pyramidal cells are regulated by different but interacting inhibitory interneurons, some of which use GABA as a neurotransmitter. The activity of these interneurons is in turn controlled by descending feedback systems.     

Behavioral parasitology and perspectives on miracidial host-finding.

This paper proposes and outlines a new interdiscipline, 'behavioral parasitology,' and presents some interpretations in one of the leading themes of this field, miracidial chemosensitivity to snails. Controversies over miracidial attraction and species-specificity are considered from the standpoints of the distinction between taxis and kinesis, the need for a stimulus gradient, and the possibility of an early phase in a miracidium's behavior adapted for dispersal rather than host-finding. Some of the many possible organic stimulants are discussed with regard to quantitative production by snails, sensory thresholds of the parasites, and possible interaction with inorganic ions. Organic and inorganic stimulants are considered to possibly form qualitative as well as quantitative gradients. A thermodynamic interpretation of miracidial klinokinesis as a function of stimulant concentration suggests the existence of two or more separate types of receptors for the same stimulant, one with a higher affinity for the stimulant and mediating a weaker klinokinesis (possibly a long-range receptor as compared to the other.     

Information transmission by isolated frog muscle spindle

Transmission of sensory information was calculated for the isolated frog muscle spindle receptor, using Shannon's information measure. Sinusoidal movements, random noise stretches, and sinusoids with superimposed auxiliary noise were applied as stimuli. In addition, the static prestretch level of the intrafusal muscle bundle was adjusted between resting length (L0) and L0 + 600 micron, so that the analysis of the information transmission properties covered the entire dynamic range of the sensory receptor organ. Sinusoidal stretches below 2 Hz evoked smoothly modulated cycle histograms, which were approximately linearly related to the stimulating sinewave. The transinformation rates under these conditions were generally low (5-17 bit X s-1), regardless of the amplitude of the applied movement. Increasing prestretch enhanced the modulation depth of the cycle histograms considerably, but increased the transinformation rates by less than 10 bit X s-1. By contrast, sinusoids above 2 Hz evoked clearly nonlinear cycle histograms, because each action potential was firmly phase-locked to a small segment of the stretch cycle. Under these conditions the transinformation rates grew larger with increasing stimulus frequency and approached 130 bit X s-1 at 60 Hz. Small amplitude sinusoidal stretches, however, evoked considerable transinformation rates in the high frequency region only then, when the spindle receptor was extended to higher prestretch levels. Random stretches evoked transinformation rates between 5 and 30 bit X s-1 depending on both the prestretch level and the intensity of the noise stimulus. The linear response components carried only about 25% of the transinformation rates transmitted by both the linear and nonlinear response components. Auxiliary noise stimuli greatly improved the information transmission of sinusoidal stretches. For example, a pure sinusoid evoked 5 bit X s-1. Adding a noise signal with equal energy to the sinusoidal movement elicited 20 bit X s-1. This facilitation effect of auxiliary noise was restricted to low frequency sinusoidal stimuli. The present results are discussed with respect to the information transmission properties of various sensory systems evaluated by either the same or different information processing procedure as that used in the present study. The functional significance of high transinformation rates sent by the muscle spindle to the central nervous system is discussed with respect to motor control.     

Repetitive stimulation of olfactory receptor cells in female silkmoths Bombyx mori L

The pheromone-sensitive receptor cells of male moth antennae are capable of detecting the rapid changes in stimulus intensity encountered in natural pheromone odour plumes. We investigated temporal response characteristics of the two receptor cell types of the sensillum trichodeum of female Bombyx mori, which are most sensitive to benzoic acid and 2,6-dimethyl-5-heptene-2-ol (DMH), respectively. The cells were repetitively stimulated with 50-ms pulses of benzoic acid and (±)-linalool, an effective mimic of DMH, at various pulse rates and different stimulus intensities. By recording receptor potentials and nerve impulses we demonstrated that both receptor cell types were able to follow stimulus pulses at least up to eight pulses per sec, with a more pronounced modulation of the responses in the DMH cell. The resolution capability of the two cell types showed little dependence on stimulus intensity. In their ability to resolve pulsed odour stimuli, the receptor cells for benzoic acid and DMH were as good as pheromone receptor cells.