Neural Dynamics of Learning Sound—Action Associations

A motor component is pre-requisite to any communicative act as one must inherently move to communicate. To learn to make a communicative act, the brain must be able to dynamically associate arbitrary percepts to the neural substrate underlying the pre-requisite motor activity. We aimed to investigate whether brain regions involved in complex gestures (ventral pre-motor cortex, Brodmann Area 44) were involved in mediating association between novel abstract auditory stimuli and novel gestural movements. In a functional resonance imaging (fMRI) study we asked participants to learn associations between previously unrelated novel sounds and meaningless gestures inside the scanner. We use functional connectivity analysis to eliminate the often present confound of ‘strategic covert naming’ when dealing with BA44 and to rule out effects of non-specific reductions in signal. Brodmann Area 44, a region incorporating Broca''s region showed strong, bilateral, negative correlation of BOLD (blood oxygen level dependent) response with learning of sound-action associations during data acquisition. Left-inferior-parietal-lobule (l-IPL) and bilateral loci in and around visual area V5, right-orbital-frontal-gyrus, right-hippocampus, left-para-hippocampus, right-head-of-caudate, right-insula and left-lingual-gyrus also showed decreases in BOLD response with learning. Concurrent with these decreases in BOLD response, an increasing connectivity between areas of the imaged network as well as the right-middle-frontal-gyrus with rising learning performance was revealed by a psychophysiological interaction (PPI) analysis. The increasing connectivity therefore occurs within an increasingly energy efficient network as learning proceeds. Strongest learning related connectivity between regions was found when analysing BA44 and l-IPL seeds. The results clearly show that BA44 and l-IPL is dynamically involved in linking gesture and sound and therefore provides evidence that one of the mechanisms required for the evolution of human communication is found within these motor regions.     

Beat gestures influence which speech sounds you hear

Beat gestures—spontaneously produced biphasic movements of the hand—are among the most frequently encountered co-speech gestures in human communication. They are closely temporally aligned to the prosodic characteristics of the speech signal, typically occurring on lexically stressed syllables. Despite their prevalence across speakers of the world''s languages, how beat gestures impact spoken word recognition is unclear. Can these simple ‘flicks of the hand'' influence speech perception? Across a range of experiments, we demonstrate that beat gestures influence the explicit and implicit perception of lexical stress (e.g. distinguishing OBject from obJECT), and in turn can influence what vowels listeners hear. Thus, we provide converging evidence for a manual McGurk effect: relatively simple and widely occurring hand movements influence which speech sounds we hear.     

The Case of Watson vs. James: Effect-Priming Studies Do Not Support Ideomotor Theory

In this paper we show that response facilitation in choice reaction tasks achieved by priming the (previously perceived) effect is based on stimulus-response associations rather than on response-effect associations. The reduced key-press response time is not accounted for by earlier established couplings between the key-press movement and its subsequent effect, but instead results from couplings between this effect and the contingent key-release movement. This key-release movement is an intrinsic part of the entire performed response action in each trial of a reaction-time task, and always spontaneously follows the key-press movement. Eliminating the key-release movement from the task leads to the disappearance of the response facilitation, which raises the question whether response-effect associations actually play a role in studies that use the effect-priming paradigm. Together the three experiments presented in the paper cast serious doubts on the claim that action-effect couplings are acquired and utilized by the cognitive system in the service of action selection, and that the priming paradigm by itself can provide convincing evidence for this claim. As a corollary, we question whether the related two-step model for the ideomotor principle holds a satisfying explanation for how anticipation of future states guides action planning. The results presented here may have profound implications for priming studies in other disciplines of psychology as well.     

A Comparative Study of Relational Learning Capacity in Honeybees (Apis mellifera) and Stingless Bees (Melipona rufiventris)

Background

Learning of arbitrary relations is the capacity to acquire knowledge about associations between events or stimuli that do not share any similarities, and use this knowledge to make behavioural choices. This capacity is well documented in humans and vertebrates, and there is some evidence it exists in the honeybee (Apis mellifera). However, little is known about whether the ability for relational learning extends to other invertebrates, although many insects have been shown to possess excellent learning capacities in spite of their small brains.

Methodology/Principal Findings

Using a symbolic matching-to-sample procedure, we show that the honeybee Apis mellifera rapidly learns arbitrary relations between colours and patterns, reaching 68.2% correct choice for pattern-colour relations and 73.3% for colour-pattern relations. However, Apis mellifera does not transfer this knowledge to the symmetrical relations when the stimulus order is reversed. A second bee species, the stingless bee Melipona rufiventris from Brazil, seems unable to learn the same arbitrary relations between colours and patterns, although it exhibits excellent discrimination learning.

Conclusions/Significance

Our results confirm that the capacity for learning arbitrary relations is not limited to vertebrates, but even insects with small brains can perform this learning task. Interestingly, it seems to be a species-specific ability. The disparity in relational learning performance between the two bee species we tested may be linked to their specific foraging and recruitment strategies, which evolved in adaptation to different environments.     

Stress-Induced Antinociception in Fish Reversed by Naloxone

Pain perception in non-mammalian vertebrates such as fish is a controversial issue. We demonstrate that, in the fish Leporinus macrocephalus, an imposed restraint can modulate the behavioral response to a noxious stimulus, specifically the subcutaneous injection of 3% formaldehyde. In the first experiment, formaldehyde was applied immediately after 3 or 5 min of the restraint. Inhibition of the increase in locomotor activity in response to formaldehyde was observed, which suggests a possible restraint-induced antinociception. In the second experiment, the noxious stimulus was applied 0, 5, 10 and 15 min after the restraint, and both 3 and 5 min of restraint promoted short-term antinociception of approximately 5 min. In experiments 3 and 4, an intraperitoneal injection of naloxone (30 mg.kg⁻¹) was administered 30 min prior to the restraint. The 3- minute restraint-induced antinociception was blocked by pretreatment with naloxone, but the corresponding 5-minute response was not. One possible explanation for this result is that an opioid and a non-preferential μ–opioid and/or non-opioid mechanism participate in this response modulation. Furthermore, we observed that both the 3- and 5- minutes restraint were severely stressful events for the organism, promoting marked increases in serum cortisol levels. These data indicate that the response to a noxious stimulus can be modulated by an environmental stressor in fish, as is the case in mammals. To our knowledge, this study is the first evidence for the existence of an endogenous antinociceptive system that is activated by an acute standardized stress in fish. Additionally, it characterizes the antinociceptive response induced by stress in terms of its time course and the opioid mediation, providing information for understanding the evolution of nociception modulation.     

In Situ Mortality Experiments with Juvenile Sea Bass (Dicentrarchus labrax) in Relation to Impulsive Sound Levels Caused by Pile Driving of Windmill Foundations

Impact assessments of offshore wind farm installations and operations on the marine fauna are performed in many countries. Yet, only limited quantitative data on the physiological impact of impulsive sounds on (juvenile) fishes during pile driving of offshore wind farm foundations are available. Our current knowledge on fish injury and mortality due to pile driving is mainly based on laboratory experiments, in which high-intensity pile driving sounds are generated inside acoustic chambers. To validate these lab results, an in situ field experiment was carried out on board of a pile driving vessel. Juvenile European sea bass (Dicentrarchus labrax) of 68 and 115 days post hatching were exposed to pile-driving sounds as close as 45 m from the actual pile driving activity. Fish were exposed to strikes with a sound exposure level between 181 and 188 dB re 1 µPa².s. The number of strikes ranged from 1739 to 3067, resulting in a cumulative sound exposure level between 215 and 222 dB re 1 µPa².s. Control treatments consisted of fish not exposed to pile driving sounds. No differences in immediate mortality were found between exposed and control fish groups. Also no differences were noted in the delayed mortality up to 14 days after exposure between both groups. Our in situ experiments largely confirm the mortality results of the lab experiments found in other studies.     

Complementary Hand Responses Occur in Both Peri- and Extrapersonal Space

Human beings have a strong tendency to imitate. Evidence from motor priming paradigms suggests that people automatically tend to imitate observed actions such as hand gestures by performing mirror-congruent movements (e.g., lifting one’s right finger upon observing a left finger movement; from a mirror perspective). Many observed actions however, do not require mirror-congruent responses but afford complementary (fitting) responses instead (e.g., handing over a cup; shaking hands). Crucially, whereas mirror-congruent responses don''t require physical interaction with another person, complementary actions often do. Given that most experiments studying motor priming have used stimuli devoid of contextual information, this space or interaction-dependency of complementary responses has not yet been assessed. To address this issue, we let participants perform a task in which they had to mirror or complement a hand gesture (fist or open hand) performed by an actor depicted either within or outside of reach. In three studies, we observed faster reaction times and less response errors for complementary relative to mirrored hand movements in response to open hand gestures (i.e., ‘hand-shaking’) irrespective of the perceived interpersonal distance of the actor. This complementary effect could not be accounted for by a low-level spatial cueing effect. These results demonstrate that humans have a strong and automatic tendency to respond by performing complementary actions. In addition, our findings underline the limitations of manipulations of space in modulating effects of motor priming and the perception of affordances.     

Priming Intelligent Behavior: An Elusive Phenomenon

Can behavior be unconsciously primed via the activation of attitudes, stereotypes, or other concepts? A number of studies have suggested that such priming effects can occur, and a prominent illustration is the claim that individuals'' accuracy in answering general knowledge questions can be influenced by activating intelligence-related concepts such as professor or soccer hooligan. In 9 experiments with 475 participants we employed the procedures used in these studies, as well as a number of variants of those procedures, in an attempt to obtain this intelligence priming effect. None of the experiments obtained the effect, although financial incentives did boost performance. A Bayesian analysis reveals considerable evidential support for the null hypothesis. The results conform to the pattern typically obtained in word priming experiments in which priming is very narrow in its generalization and unconscious (subliminal) influences, if they occur at all, are extremely short-lived. We encourage others to explore the circumstances in which this phenomenon might be obtained.     

Neural correlates of knowledge: stable representation of stimulus associations across variations in behavioral performance

Behavioral responses to a sensory stimulus are often guided by associative memories. These associations remain intact even when other factors determine behavior. The substrates of associative memory should therefore be identifiable by neuronal responses that are independent of behavioral choices. We tested this hypothesis using a paired-associates task in which monkeys learned arbitrary associations between pairs of visual stimuli. We examined the activity of neurons in inferior temporal cortex as the animals prepared to choose a remembered stimulus from a visual display. The activity of some neurons (22%) depended on the monkey's behavioral choice; but for a novel class of neurons (54%), activity reflected the stimulus that the monkey was instructed to choose, regardless of the behavioral response. These neurons appear to represent memorized stimulus associations that are stable across variations in behavioral performance. In addition, many neurons (74%) were modulated by the spatial arrangement of the stimuli in the display.     

Evidence for perception of fine echo delay and phase by the FM bat,Eptesicus fuscus

The big brown bat, Eptesicus fuscus, can perceive small changes in the delay of FM sonar echoes and shifts in echo phase, which interact with delay. Using spectral cues caused by interference, Eptesicus also can perceive the individual delays of two overlapping FM echoes at small delay separations. These results have been criticized as due to spectral artifacts caused by overlap between stimulus echoes and extraneous sounds (Pollak 1993). However, no amplitude or spectral variations larger than 0.05 dB accompany delay or phase changes produced by the electronic apparatus. No reverberation falls in the narrow span of delays required to produce the bat's performance curve from echo interference cues. Consistent differences in the durations of sonar sounds for 6 bats that perform the same in the experiments demonstrate that overlap between stimulus echoes and extraneous echoes is not necessary, and changes in the amount of echo overlap have no effect on performance. Noise-induced random variations in echo spectra outweigh putative spectral artifacts, and deliberately-introduced spectral artifacts do not improve performance overall but instead yield new time-frequency images. Amplitude-latency trading of perceived delay, proposed as a demonstration that the latency of neural discharges encodes delay (Pollak et al. 1977), confirms that the bat's fine delay and phase perception depends on a temporal neural code. The perceived delays depend on stimulus delays, not the delays of extraneous sounds. The rejected criticisms are based on physiological results with random-phase FM stimuli which are irrelevant to neural coding of fine echo delay and phase.The contents of this paper first appeared in October 1990 in a letter to G.D. Pollak in response to his unpublished criticisms of echo-jitter experiments. These responses also have been presented at the 1991 and 1992 Association for Research in Otolaryngology midwinter meetings and at the 1992 3rd International Congress of Neuroethology. Several of the control experiments also appeared in Simmons et al. (1990b). The now-published criticisms (Pollak 1993, the preceding paper) have not addressed these responses, including the prior published data demonstrating that the stimulus conditions asserted by these criticisms do not in fact occur.     

Two Failures to Replicate High-Performance-Goal Priming Effects

Bargh et al. (2001) reported two experiments in which people were exposed to words related to achievement (e.g., strive, attain) or to neutral words, and then performed a demanding cognitive task. Performance on the task was enhanced after exposure to the achievement related words. Bargh and colleagues concluded that better performance was due to the achievement words having activated a "high-performance goal". Because the paper has been cited well over 1100 times, an attempt to replicate its findings would seem warranted. Two direct replication attempts were performed. Results from the first experiment (n = 98) found no effect of priming, and the means were in the opposite direction from those reported by Bargh and colleagues. The second experiment followed up on the observation by Bargh et al. (2001) that high-performance-goal priming was enhanced by a 5-minute delay between priming and test. Adding such a delay, we still found no evidence for high-performance-goal priming (n = 66). These failures to replicate, along with other recent results, suggest that the literature on goal priming requires some skeptical scrutiny.     

Responses to Playback of Local vs. Distant Contact Calls in the Orange-Fronted Conure, Aratinga canicularis

We conducted interactive playback experiments on foraging flocks of orange‐fronted conures, Aratinga canicularis, using loud contact calls that had been recorded at sites ranging from 0 to 30 km from the playback site. Responses were scored on the basis of the proximity of approach to the speaker, the number of different vocalizations produced by the responding flock, and the duration of respondent vocal interactions with the playbacks. Overall response strength decreased significantly as distance between playback and recording sites was increased up to 9 km, and remained at a steady low level for greater distances. As 9 km is the upper limit of conure home ranges measured in this study site, this nonlinear effect of response with distance suggests that response strength is partly determined by familiarity with calls of local birds. An additional and independent amount of the variation in response strength was explained by the structural similarity between respondent and stimulus calls. This correlation could be caused by a preference to interact with known stimulus birds whose calls have converged during prior associations. However, our data suggest that responding birds subtly changed their call structure during longer trials to more closely match the stimulus call. If subsequently verified as a common phenomenon, this finding could provide an important explanation for the remarkable imitative abilities of parrots.     

Training a new response using conditioned reinforcement

Some of the most frequently used methods in the study of conditioned reinforcement seem to be insufficient to demonstrate the effect. The clearest way to assess this phenomenon is the training of a new response. In the present study, rats were exposed to a situation in which a primary reinforcer and an arbitrary stimulus were paired and subsequently the effect of this arbitrary event was assessed by presenting it following a new response. Subjects under these conditions emitted more responses compared to their own responding before the pairing and to their responding on a similar operandum that was available concurrently that had no programmed consequences. Response rates also were higher compared to responding by subjects in similar conditions in which there was no contingency (a) between the arbitrary stimulus and the reinforcer, (b) between the response and the arbitrary stimulus or (c) both. Results are discussed in terms of necessary and sufficient conditions to study conditioned reinforcement.     

The psychophysics of concurrent sound segregation.

To perceptually separate concurrent complex sounds, normally hearing listeners simultaneously combine information across a wide range of frequency components. Three psychoacoustical experiments are described which investigate different forms of this across-frequency processing. The first two experiments investigate the role of coherence of frequency modulation (FM) between widely separated frequency components of a complex sound. The first experiment bolsters existing evidence that, for harmonic sounds, listeners can discriminate coherent from incoherent FM, but only by detecting the mistuning that arises from incoherent FM. The second demonstrates that, for inharmonic sounds, coherence of FM has no effect on the phenomenon of modulation detection interference (see Moore & Shailer, this symposium) once within-channel cues (combination tones and beating) are masked by background noise. It is concluded that there is not an across-frequency mechanism specific to the detection of FM incoherence. The third experiment investigates the extent to which the detection of mistuning of one component of a harmonic complex is impaired by an interfering sound (the 'interferer') with a frequency spectrum similar to that of the mistuned component. When the interferer is gated on and off with the harmonic complex, it has only a small effect provided that its level is more than 3 dB below that of the target. However, when the interferer starts before and ends after the complex, thresholds are elevated more, and this elevation occurs even for low-level interferers. Explanations of this effect in terms of adaptation and of auditory streaming are discussed.     

An electrophysiological study of sound sensitive neurons in the ‘Primitive ear’ of Acheta domesticus

Crickets have two types of mechanisms for the reception of environmental sounds: (1) the tympanal organs in the two forelegs and (2) the freely articulated setal receptors on the abdominal ceri. The cercal setal receptors have hitherto received much less experimental attention as decoders of biologically significant sounds than have the tympano-receptors. In the present study the cercal auditory system of Acheta domesticus was examined electrophysiologically to determine its auditory frequency sensitivity, the tuning characteristics of individual units, and the synchronization between nerve impulses and stimulus frequency. Both pre- and postsynaptic units were examined in the fifth abdominal ganglion; several of the observed response patterns were compared with those of homologous cercal sensory neurons in Periplaneta americana. The results show that (1) A. domesticus possesses an elaborate array of cercal receptors which are highly sensitive to sounds, (2) the cercal setal receptors are more sensitive and numerous in the cricket than in the cockroach, and (3) the cercal auditory system can decode stimulus information by narrow tuning in individual cells and by synchronous discharge patterns; firing frequencies range up to 300 Hz in presynaptic sensory units and 60 Hz in the postsynaptic giants. The response patterns were related to the structure of the receptor and the behavioural adaptations of the insect.     

Prospective timing in pigeons: Isolating temporal perception in the time-left procedure

In the time-left procedure, a task used to study prospective timing, animals choose between two stimuli that signal different delays to reinforcement. Trials begin with one stimulus signaling C seconds to reinforcement and, at different moments since its onset, another stimulus, signaling S seconds to reinforcement, with C > S, is introduced. Optimal performance consists in choosing the stimulus signaling the shorter time to reinforcement. Animals have been found to perform in this optimal way. However, this procedure is complex and variables other than time may be responsible for the results. In two experiments with pigeons we sought to improve the time-left procedure to better isolate the effect of time in the animals’ behavior. We attempted to control for two confounding variables, the asymmetry in the time markers from training to testing and the cost of switching between the two response alternatives. We conclude that in the time-left task pigeons seem indeed to regulate their behavior based on time because, with our improved procedure, they still chose the stimulus associated with the shorter time to food. However, our version of the procedure created new interpretative difficulties, strengthening the idea that the time-left procedure may be too complex to study timing.     

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.     

Echoes of the spoken past: how auditory cortex hears context during speech perception

What do we hear when someone speaks and what does auditory cortex (AC) do with that sound? Given how meaningful speech is, it might be hypothesized that AC is most active when other people talk so that their productions get decoded. Here, neuroimaging meta-analyses show the opposite: AC is least active and sometimes deactivated when participants listened to meaningful speech compared to less meaningful sounds. Results are explained by an active hypothesis-and-test mechanism where speech production (SP) regions are neurally re-used to predict auditory objects associated with available context. By this model, more AC activity for less meaningful sounds occurs because predictions are less successful from context, requiring further hypotheses be tested. This also explains the large overlap of AC co-activity for less meaningful sounds with meta-analyses of SP. An experiment showed a similar pattern of results for non-verbal context. Specifically, words produced less activity in AC and SP regions when preceded by co-speech gestures that visually described those words compared to those words without gestures. Results collectively suggest that what we ‘hear’ during real-world speech perception may come more from the brain than our ears and that the function of AC is to confirm or deny internal predictions about the identity of sounds.     

Identity Negative Priming: A Phenomenon of Perception,Recognition or Selection?

The present study addresses the problem whether negative priming (NP) is due to information processing in perception, recognition or selection. We argue that most NP studies confound priming and perceptual similarity of prime-probe episodes and implement a color-switch paradigm in order to resolve the issue. In a series of three identity negative priming experiments with verbal naming response, we determined when NP and positive priming (PP) occur during a trial. The first experiment assessed the impact of target color on priming effects. It consisted of two blocks, each with a different fixed target color. With respect to target color no differential priming effects were found. In Experiment 2 the target color was indicated by a cue for each trial. Here we resolved the confounding of perceptual similarity and priming condition. In trials with coinciding colors for prime and probe, we found priming effects similar to Experiment 1. However, trials with a target color switch showed such effects only in trials with role-reversal (distractor-to-target or target-to-distractor), whereas the positive priming (PP) effect in the target-repetition trials disappeared. Finally, Experiment 3 split trial processing into two phases by presenting the trial-wise color cue only after the stimulus objects had been recognized. We found recognition in every priming condition to be faster than in control trials. We were hence led to the conclusion that PP is strongly affected by perception, in contrast to NP which emerges during selection, i.e., the two effects cannot be explained by a single mechanism.