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.     

The habituation of event-related potentials to speech sounds and tones

We examined the short- and long-term habituation of auditory event-related potentials (ERPs) elicited by tones, complex tones and digitized speech sounds (vowels and consonant-vowel-consonant syllables). Twelve different stimuli equated in loudness and duration (300 msec) were studied. To examine short-term habituation stimuli were presented in trains of 6 with interstimulus intervals of 0.5 or 1.0 sec. The first 4 stimuli in a train were identical standards. On 50% of the trains the standard in the 5th position was replaced by a deviant probe stimulus, and on 20% of the trains the standard in the 6th position was replaced by a target, a truncated standard that required a speeded button press response.Short-term habituation (STH) was complete by the third stimulus in the train and resulted in amplitude decrements of 50–75% for the N1 component. STH was partially stimulus specific in that amplitudes were larger following deviant stimuli in the 5th position than following standards. STH of the N1 was more marked for speech sounds than for loudness-matched tones or complex tones at short ISI. In addition, standard and deviant stimuli that differed in phonetic structure showed more cross-habituation than did tones or complex tones that differed in frequency. This pattern of results suggests that STH is a function of the acoustic resemblance of successive stimuli.The long-term habituation (LTH) of the ERP was studied by comparing amplitudes across balanced 5.25 m stimulus blocks over the course of the experiment. Two types of LTH were observed. The N1 showed stimulus-specific LTH in that N1 amplitudes declined during the presentation of a stimulus, but returned to control levels when a different stimulus was presented in the subsequent condition. In contrast, the P3 elicited by the deviant stimuli showed non-specific LTH, being reduced across successive blocks containing different stimuli. P3s elicited by target stimuli remained stable in amplitude.     

Intracellular stimulation of sensory cells elicits swimming activity in the medicinal leech

Intracellular stimulation of each of three different types of mechanoreceptors, the T, P and N cells, evokes swimming behavior in leech preparations. Stimulation of an individual N cell or P cell evoked swimming in 75% and 53% respectively, of the preparations tested. Stimulation of an individual T cell was ineffective in eliciting swimming; however, simultaneous stimulation of two T cells evoked swimming in 59% of our preparations. Stimulation of mechanosensory neurons elicited swimming activity for a limited number of trials; i.e. the response habituated. The number of swim episodes evoked before habituation to criterion did not differ significantly for the different types of mechanoreceptors. The duration of swim episodes declined significantly over the course of N cell stimulation. The tendency for swim length to decline with repeated stimulation was present as well for swim episodes elicited by P or T cell stimulation. Swim initiation recovered spontaneously following habituation resulting from T cell stimulation. Spontaneous recovery following N cell stimulation was not demonstrated. However, N cell stimulation evoked swimming again after DP nerve shock or to a limited extent, after cell 204 stimulation. Spontaneous recovery of swim initiation to P cell stimulation was not investigated. A previous study detailed habituation of swimming activity to mechanical stimulation of the body wall (Debski and Friesen 1985). Only the T cells are activated significantly by this stimulus. Stimulation of sensory receptors other than mechanoreceptors was not effective in eliciting swimming in our preparation. We conclude that T cells mediate swim initiation elicited by stroking of the body wall and that the cessation of swimming to this stimulus is not due to sensory adaptation.     

Activation of duration-sensitive auditory cortical fields in humans

The influence of stimulus duration on auditory evoked potentials (AEPs) was examined for tones varying randomly in duration, location, and frequency in an auditory selective attention task. Stimulus duration effects were isolated as duration difference waves by subtracting AEPs to short duration tones from AEPs to longer duration tones of identical location, frequency and rise time. This analysis revealed that AEP components generally increased in amplitude and decreased in latency with increments in signal duration, with evidence of longer temporal integration times for lower frequency tones. Different temporal integration functions were seen for different N1 subcomponents. The results suggest that different auditory cortical areas have different temporal integration times, and that these functions vary as a function of tone frequency.     

Mechanical basis of otoacoustic emissions in tympanal hearing organs

Tympanal hearing organs of insects emit distortion–product otoacoustic emissions (DPOAEs), which in mammals are used as indicator for nonlinear cochlear amplification, and which are highly vulnerable to manipulations interfering with the animal’s physiological state. Although in previous studies, evidence was provided for the involvement of auditory mechanoreceptors, the source of DPOAE generation and possible active mechanisms in tympanal organs remained unknown. Using laser Doppler vibrometry in the locust ear, we show that DPOAEs mechanically emerge at the tympanum region where the auditory mechanoreceptors are attached. Those emission-coupled vibrations differed remarkably from tympanum waves evoked by external pure tones of the same frequency, in terms of wave propagation, energy distribution, and location of amplitude maxima. Selective inactivation of the auditory receptor cells by mechanical lesions did not affect the tympanum’s response to external pure tones, but abolished the emission’s displacement amplitude peak. These findings provide evidence that tympanal auditory receptors, comparable to the situation in mammals, comprise the required nonlinear response characteristics, which during two-tone stimulation lead to additional, highly localized deflections of the tympanum.     

Auditory evoked responses to rhythmic sound pulses in dolphins

The ability of auditory evoked potentials to follow sound pulse (click or pip) rate was studied in bottlenosed dolphins. Sound pulses were presented in 20-ms rhythmic trains separated by 80-ms pauses. Rhythmic click or pip trains evoked a quasi-sustained response consisting of a sequence of auditory brainstem responses. This was designated as the rate-following response. Rate following response peak-to-peak amplitude dependence on sound pulse rate was almost flat up to 200 s⁻¹, then displayed a few peaks and valleys superimposed on a low-pass filtering function with a cut-off frequency of 1700 s⁻¹ at a 0.1-amplitude level. Peaks and valleys of the function corresponded to the pattern of the single auditory brain stem response spectrum; the low-pass cut-off frequency was below the auditory brain stem response spectrum bandwidth. Rate-following response frequency composition (magnitudes of the fundamental and harmonics) corresponded to the auditory brain stem response frequency spectrum except for lower fundamental magnitudes at frequencies above 1700 Hz. These regularities were similar for both click and pip trains. The rate-following response to steady-state rhythmic stimulation was similar to the rate-following response evoked by short trains except for a slight amplitude decrease with the rate increase above 10 s⁻¹. The latter effect is attributed to a long-term rate-dependent adaptation in conditions of the steady-state pulse stimulation. Accepted: 18 June 1998     

Electrically-Evoked Frequency-Following Response (EFFR) in the Auditory Brainstem of Guinea Pigs

It is still a difficult clinical issue to decide whether a patient is a suitable candidate for a cochlear implant and to plan postoperative rehabilitation, especially for some special cases, such as auditory neuropathy. A partial solution to these problems is to preoperatively evaluate the functional integrity of the auditory neural pathways. For evaluating the strength of phase-locking of auditory neurons, which was not reflected in previous methods using electrically evoked auditory brainstem response (EABR), a new method for recording phase-locking related auditory responses to electrical stimulation, called the electrically evoked frequency-following response (EFFR), was developed and evaluated using guinea pigs. The main objective was to assess feasibility of the method by testing whether the recorded signals reflected auditory neural responses or artifacts. The results showed the following: 1) the recorded signals were evoked by neuron responses rather than by artifact; 2) responses evoked by periodic signals were significantly higher than those evoked by the white noise; 3) the latency of the responses fell in the expected range; 4) the responses decreased significantly after death of the guinea pigs; and 5) the responses decreased significantly when the animal was replaced by an electrical resistance. All of these results suggest the method was valid. Recording obtained using complex tones with a missing fundamental component and using pure tones with various frequencies were consistent with those obtained using acoustic stimulation in previous studies.     

Transfer of habituation in Aplysia: contribution of heterosynaptic pathways in habituation of the gill-withdrawal reflex

Habituation of the Aplysia gill-withdrawal reflex (and siphon-withdrawal reflex) has been attributed to low-frequency homosynaptic depression at central sensory-motor synapses. The recent demonstration that transfer of habituation between stimulation sites occurs in this model system has prompted the hypothesis that heterosynaptic inhibitory pathways also play a role in the mediation of habituation behavior. To test this hypothesis, the sites and mechanisms of neural plasticity which underlie transfer of habituation in Aplysia were examined. Transfer of habituation is a reduction in the reflex evoked at one stimulation site (siphon) due to repeated presentation of a stimulus to a second site (gill). Centrally mediated transfer of habituation, measured in a preparation lacking the siphon-gill peripheral nervous system (PNS), was associated with a reduced excitatory response in central motor neurons. Repeated tactile stimulation of the gill did not attenuate the gill response evoked by electrical stimulation of the branchial nerve nor the mechanoreceptor response recorded in LE sensory neurons. In contrast, repeated stimulation of siphon or gill at a site which was "off" the sensory field of a specific mechanoreceptor led to a diminution in synaptic transmission between that sensory neuron and its followers (motor neurons and inter-neurons). These data demonstrate that centrally mediated transfer of habituation results from heterosynaptic modulation of synaptic transmission at the sensory-motor (and sensory-interneuron) synapses. Therefore, habituation behavior in Aplysia is mediated through the conjoint action of homosynaptic and heterosynaptic inhibitory processes.     

The development of central nervous system control of the gill withdrawal reflex evoked by siphon stimulation in Aplysia

In older Aplysia, the central nervous system (CNS) (abdominal ganglion) exerts suppressive and facilitatory control over the peripheral nervous system (PNS) which initially mediates the gill withdrawal reflex and its subsequent habituation evoked by tactile stimulation of the siphon. In young animals, both the suppressive and facilitatory CNS control were found to be absent. In older animals, removal of branchial nerve (Br) input to the gill resulted in a significantly reduced reflex latency and, with ctenidial (Ct) and siphon (Sn) nerves intact, a significantly increased reflex amplitude and an inability of the reflex to habituate with repeated siphon stimulation. In young animals, removal of Br had no effect on reflex latency and with Ct and Sn intact, the reflex amplitude latency was not increased and the reflex habituated. Older animals can easily discriminate between different intensity stimuli applied to the siphon as evidenced by differences in reflex amplitude, rates of habituation, and evoked neural activity. On the other hand, young animals cannot discriminate well between different stimulus intensities. The lack of CNS control in young animals was found to be due to incompletely developed neural processes within the abdominal ganglion and not the PNS. The lack of CNS control in young Aplysia results in gill reflex behaviours being less adaptive in light of changing stimulus conditions, but may be of positive survival value in that the young will not habituate as easily. The fact that CNS control is present in older animals strengthens the idea that in any analysis of the underlying neural mechanisms of habituation the entire integrated CNS-PNS must be taken into account.     

Stimulus-specific adaptation and deviance detection in the rat auditory cortex

Stimulus-specific adaptation (SSA) is the specific decrease in the response to a frequent ('standard') stimulus, which does not generalize, or generalizes only partially, to another, rare stimulus ('deviant'). Stimulus-specific adaptation could result simply from the depression of the responses to the standard. Alternatively, there may be an increase in the responses to the deviant stimulus due to the violation of expectations set by the standard, indicating the presence of true deviance detection. We studied SSA in the auditory cortex of halothane-anesthetized rats, recording local field potentials and multi-unit activity. We tested the responses to pure tones of one frequency when embedded in sequences that differed from each other in the frequency and probability of the tones composing them. The responses to tones of the same frequency were larger when deviant than when standard, even with inter-stimulus time intervals of almost 2 seconds. Thus, SSA is present and strong in rat auditory cortex. SSA was present even when the frequency difference between deviants and standards was as small as 10%, substantially smaller than the typical width of cortical tuning curves, revealing hyper-resolution in frequency. Strong responses were evoked also by a rare tone presented by itself, and by rare tones presented as part of a sequence of many widely spaced frequencies. On the other hand, when presented within a sequence of narrowly spaced frequencies, the responses to a tone, even when rare, were smaller. A model of SSA that included only adaptation of the responses in narrow frequency channels predicted responses to the deviants that were substantially smaller than the observed ones. Thus, the response to a deviant is at least partially due to the change it represents relative to the regularity set by the standard tone, indicating the presence of true deviance detection in rat auditory cortex.     

The recovery functions of auditory event-related potentials during split-second discriminations

We examined the recovery cycles of auditory event-related potentials (ERPs) in a high-speed auditory discrimination task and in passive conditions. Each trial contained 3 tones cued by a warning flash. In passive conditions, auditory ERPs consisted mainly of N1 (108 msec) and P2 (213 msec) components superimposed on a small CNV. The N1 and P2 were comparable in amplitude and both had prolonged refractory periods. In discriminative reaction time (DRT) conditions the same tones cued or inhibited press responses and elicited additional endogenous components (principally the Nd and P3). ERPs in DRT conditions were superimposed upon a prominent CNV that began after the warning cue and lasted throughout the signal delivery period.The N1 was larger in active than passive conditions and showed less marked refractory effects, while the P2 was smaller and showed more marked refractoriness. Differences between active and passive conditions could be explained by the presence of an endogenous negative potential (the Nd) with a short refractory period that was superimposed upon the N1 and P2.The P3 was recorded only in active conditions. At short ISIs (0.5 sec), P3 amplitudes were reduced and P3 latencies lengthened in parallel with prolongations in reaction time due to so-called psychological refractory period (PRP) effects. Both P3 recovery and the PRP reflected central mechanisms since they were observed at short ISIs when stimuli cueing different responses succeeded one another.N1 and P3 amplitudes diminished over the course of the experiment in both active and passive conditions. The decrease (amounting to about 30% of initial amplitudes) did not appear due to reductions in vigilance, since it was not accompanied by changes in reaction time or response accuracy, or by changes in other endogenous components (CNV or Nd). Short-term N1 habituation was unaffected by long-term amplitude reductions suggesting that independent mechanisms were responsible for the two phenomena.     

Visual evoked potential in guinea pigs

The present study was designed to establish visual evoked potential (VEP) as one of clinical tests for veterinary medicine. Experiments were carried out on eight adult male guinea pigs weighed 350 to 750 g. We investigated influences of click sound, luminous intensity and habituation on VEP patterns. The VEP of the guinea pig was composed of primary (P 10, N 20, P 30, N 40) and secondary (P 55, N 75, P 100, N 140) components, followed by a rhythmic after-discharge. Click sound with flash produced some unclear peaks in VEP, while click sound without flash elicited clear six peaks. These different components of the response to stimulation suggested that the acoustically evoked potential induced some peaks in VEP. With the intensity used in the present study, changes in luminous intensity resulted in unrecognizable difference among the VEPs. Early components of VEP were not clearly influenced by the habituation to stimulation. As the stimulation was repeated, rhythmic after-discharge seemed to be suppressed in the half of experiments.     

Control of gill reflex habituation and the rate of EPSP decrement of L7 by a common source in the CNS of Aplysia

It was found in older Aplysia that the rate of decrement of the EPSP evoked in L₇ by repeated tactile stimulation of the gill was dependent on the strength of the applied stimulus and that the rate of decrement paralleled the rate of gill reflex habituation. As the stimulus intensity was increased both rates slowed. In contrast, it was found in young Aplysia that the rate of EPSP decrement and the rate of gill reflex habituation were independent of the strength of the stimulus applied to the gill. Neither rate changed as the stimulus intensity was changed. Moreover, L₇'s of young animals are more responsive to tactile stimuli applied to the gill than are L₇'s of older animals and the difference in excitability is not due to any differences in passive membrane properties between the L₇'s in young and older Aplysia. These findings are fully consistent with and supportive of the proposal that a common neuronal source in the parieto-visceral ganglion of Aplysia controls the rate of gill reflex habituation, the synaptic input to L₇, and the rate of decrement of this input, evoked by repeated tactile stimulation of the gill. Additinally, it was proposed that this common source is developed in completely in the young. As a consequence of this incomplete development, young Aplysia exhibit less adaptability to changing stimulus conditions and, in general, less ability to suppress their behavior. It may thus be possible to study directly developmental changes in the nervous system which act to transform juvenile behavior to adult behavior.     

Dynamics of habituation in different cortical regions of the cat brain

The dynamics of habituation in the rostral part of the parietal association region and also in the first and second somatosensory areas was studied by the evoked potentials (EP) method in cats anesthetized with chloralose (80-90 mg/kg) and immobilized with flaxedil. During repeated stimulation of the splanchnic nerve brief habituation of EP developed in the cortex. It corresponded in its basic features to habituation observed in other sensory systems. On comparison of the rates of development of habituation in the primary and secondary projection zones of the splanchnic nerve in the cortex differences were found: habituation developed more rapidly in the secondary projection zones. The functional importance of this phenomenon is discussed.     

Activation of Auditory Cortex by Anticipating and Hearing Emotional Sounds: An MEG Study

To study how auditory cortical processing is affected by anticipating and hearing of long emotional sounds, we recorded auditory evoked magnetic fields with a whole-scalp MEG device from 15 healthy adults who were listening to emotional or neutral sounds. Pleasant, unpleasant, or neutral sounds, each lasting for 6 s, were played in a random order, preceded by 100-ms cue tones (0.5, 1, or 2 kHz) 2 s before the onset of the sound. The cue tones, indicating the valence of the upcoming emotional sounds, evoked typical transient N100m responses in the auditory cortex. During the rest of the anticipation period (until the beginning of the emotional sound), auditory cortices of both hemispheres generated slow shifts of the same polarity as N100m. During anticipation, the relative strengths of the auditory-cortex signals depended on the upcoming sound: towards the end of the anticipation period the activity became stronger when the subject was anticipating emotional rather than neutral sounds. During the actual emotional and neutral sounds, sustained fields were predominant in the left hemisphere for all sounds. The measured DC MEG signals during both anticipation and hearing of emotional sounds implied that following the cue that indicates the valence of the upcoming sound, the auditory-cortex activity is modulated by the upcoming sound category during the anticipation period.     

Correlation between auditory evoked responses in the thalamus and species-specific call characteristics

This evoked potential study of the bullfrog's auditory thalamic area (an auditory responsive region in the posterior dorsal thalamus) shows that complex processing, distinct from that reported in lower auditory regions, occurs in this center. An acoustic stimulus consisting of two tones, one which stimulates either the low-frequency or the mid-frequency sensitive population of auditory nerve fibers from the amphibian papilla and the other the high-frequency sensitive population of fibers from the basilar papilla, evoked a maximal response. The amplitude of the response to the simultaneous stimulation of the two auditory organs was, in some locations, much larger than the linear sum of the responses to the individual tones presented separately. Bimodal spectral stimuli that had relatively long rise-times (greater than or equal to 100 ms) evoked much larger responses than similar sounds with short rise-times. The optimal rise-times were close to those occurring in the bullfrog's mating call. The response was dependent on the waveform periodicity and harmonic content, with a fundamental frequency of 200 Hz producing a larger response than those with fundamentals of 50, 100 or 300 Hz. Six of the natural calls in the bullfrog's vocal repertoire were tested and the mating call and warning call were found to evoke the best responses. Each of these calls stimulate the two auditory organs simultaneously. The evoked response had a long refractory period which could not be altered by lesioning the efferent telencephalic pathways. The type of spectral and temporal information extracted by the auditory thalamic area suggests that this center is involved in processing complex sounds and likely plays an important role in the bullfrog's detection of some of its vocal signals.     

Interpretation of the Repetitive Firing of Nerve Cells

Eccentric cells of Limulus respond with repetitive firing to sustained depolarizing currents. Following stimulation with a step of current, latency is shorter than first interval and later intervals increase progressively. A shock of intensity twice threshold can evoke firing 25 msec. after an impulse. But in the same cell, a current step twice rheobase evokes a second impulse more than 50 msec. after the first, and current intensity must be raised to over five times rheobase to obtain a first interval of about 25 msec. Repetitive firing was evoked by means of trains of shocks. With stimuli of moderate intensity, firing was evoked by only some of the shocks and intervals between successive impulses increased with time. This is ascribed to accumulation of refractoriness with successive impulses. Higher frequencies of firing are obtained with shocks of intensity n x threshold than with constant currents of intensity n x rheobase. It is concluded that prolonged currents depress the processes leading to excitation and that (in the cells studied) repetitive firing is controlled both by the after-effects of firing (refractoriness) and by the depressant effects of sustained stimuli (accommodation). Development of subthreshold "graded activity" is an important process leading to excitation of eccentric cells, but is not the principal factor determining frequency of firing in response to constant currents.     

Temporal integration in auditory sensory memory: neuromagnetic evidence

The cortical mechanisms of auditory sensory memory were investigated by analysis of neuromagnetic evoked responses. The major deflection of the auditory evoked field (N100m) appears to comprise an early posterior component (N100m^P) and a late anterior component (N100m^A) which is sensitive to temporal factors. When pairs of identical sounds are presented at intervals less than about 250 msec, the second sound evokes N100m^A with enhanced amplitude at a latency of about 150 msec. We suggest that N100m^A may index the activity of two distinct processes in auditory sensory memory. Its recovery cycle may reflect the activity of a memory trace which, according to previous studies, can retain processed information about an auditory sequence for about 10 sec. The enhancement effect may reflect the activity of a temporal integration process, whose time constant is such that sensation persists for 200–300 msec after stimulus offset, and so serves as a short memory store. Sound sequences falling within this window of integration seem to be coded holistically as unitary events.     

Asymmetric cortical adaptation effects during alternating auditory stimulation

The present study investigates hemispheric asymmetries in the neural adaptation processes occurring during alternating auditory stimulation. Stimuli were two monaural pure tones having a frequency of 400 or 800 Hz and a duration of 500 ms. Electroencephalogram (EEG) was recorded from 14 volunteers during the presentation of the following stimulus sequences, lasting 12 s each: 1) evoked potentials (EP condition, control), 2) alternation of frequency and ear (FE condition), 3) alternation of frequency (F condition), and 4) alternation of ear (E condition). Main results showed that in the central area of the left hemisphere (around C3 site) the N100 response underwent adaptation in all patterns of alternation, whereas in the same area of the right hemisphere the tones presented at the right ear in the FE produced no adaptation. Moreover, the responses to right-ear stimuli showed a difference between hemispheres in the E condition, which produced less adaptation in the left hemisphere. These effects are discussed in terms of lateral symmetry as a product of hemispheric, pathway and ear asymmetries.     

Habituation of auditory evoked potentials and emotional state

"Fast" and "slow" habituation of N1 and N1-P2 components of auditory evoked potentials was studied in healthy subjects and in depressed patients. In patients, initially more low amplitudes of N1 and N1-P2 were revealed, as well as slowing down of habituation in the beginning of stimuli series and acceleration to its end (in healthy people--the greatest habituation in the initial part of the series and amplitude increase at its end), the absence of power effect in the component N1 at reaching, in the process of habituation, of the same minimum parameters as in healthy subjects. This points to weakening of dishabituation process parallel with well expressed "slow" habituation in patients and allows to suggest at expressed negative emotions a deficit of attention processes as a result of "internal abstraction".