Yoshimasa Seki

Cognitive bias in rats evoked by ultrasonic vocalizations suggests emotional contagion

Emotional contagion occurs when an individual acquires the emotional state of another via social cues, and is an important component of empathy. Empathic responses seen in rodents are often explained by emotional contagion. Rats emit 50kHz ultrasonic vocalizations (USVs) in positive contexts, and emit 22kHz USVs in negative contexts. We tested whether rats show positive or negative emotional contagion after hearing conspecific USVs via a cognitive bias task. We hypothesized that animals in positive emotional states would perceive an ambiguous cue as being good (optimistic bias) whereas animals in negative states would perceive the same cue as being bad (pessimistic bias). Rats were trained to respond differently to two sounds with distinct pitches, each of which signaled either a positive or a negative outcome. An ambiguous cue with a frequency falling between the two stimuli tested whether rats interpreted it as positive or negative. Results showed that rats responded to ambiguous cues as positive when they heard the 50kHz USV (positive vocalizations) and negative when they heard the 22kHz USV (negative vocalizations). This suggests that conspecific USVs can evoke emotional contagion, both for positive and negative emotions, to change the affective states in receivers.

Songbirds and humans apply different strategies in a sound sequence discrimination task.

The abilities of animals and humans to extract rules from sound sequences have previously been compared using observation of spontaneous responses and conditioning techniques. However, the results were inconsistently interpreted across studies possibly due to methodological and/or species differences. Therefore, we examined the strategies for discrimination of sound sequences in Bengalese finches and humans using the same protocol. Birds were trained on a GO/NOGO task to discriminate between two categories of sound stimulus generated based on an “AAB” or “ABB” rule. The sound elements used were taken from a variety of male (M) and female (F) calls, such that the sequences could be represented as MMF and MFF. In test sessions, FFM and FMM sequences, which were never presented in the training sessions but conformed to the rule, were presented as probe stimuli. The results suggested two discriminative strategies were being applied: (1) memorizing sound patterns of either GO or NOGO stimuli and generating the appropriate responses for only those sounds; and (2) using the repeated element as a cue. There was no evidence that the birds successfully extracted the abstract rule (i.e., AAB and ABB); MMF-GO subjects did not produce a GO response for FFM and vice versa. Next we examined whether those strategies were also applicable for human participants on the same task. The results and questionnaires revealed that participants extracted the abstract rule, and most of them employed it to discriminate the sequences. This strategy was never observed in bird subjects, although some participants used strategies similar to the birds when responding to the probe stimuli. Our results showed that the human participants applied the abstract rule in the task even without instruction but Bengalese finches did not, thereby reconfirming that humans have to extract abstract rules from sound sequences that is distinct from non-human animals.

Song Motor control organizes acoustic patterns on two levels in Bengalese finches (Lonchura striata var. domestica)

Based on statistical analyses of song sequences, Bengalese finch (Lonchura striata var. domestica) songs do not show unvarying motif repetition as has been found in zebra finches (Taeniopygia guttata). Instead, there are variations of partially stereotyped sequences of song syllables. Although these stereotyped sequences consist of multiple syllables, in most cases these syllables occur together. To examine whether such structures really exist as a vocal production unit, we subjected singing birds to a light flash and determined when the stimulus stopped the songs. When light interruptions were presented within the statistically stereotyped sequences, the subsequent syllables tended to be produced, whereas interruptions presented during the statistically variable sequences tended to cause instantaneous song termination. This suggests that the associations among the song syllables that compose the statistically stereotyped sequences are more order dependent than those for the statistically variable sequences, and the tolerances of syllable pairs to visual interruptions are consistent with the statistical song structures. Additionally, following interruptions, several types of song sequence variations were observed that had not been previously reported. These phenomena might be caused by various effects of the visual stimulus on the hierarchical motor control program.

Effects of amygdala lesions on male mouse ultrasonic vocalizations and copulatory behaviour.

Mice produce ultrasonic vocalizations (USVs) in several behavioural contexts. In particular, male mice articulate a long series of various sounds to females during courtship behaviour. To determine the relationships between this kind of vocal behaviour and emotion, we examined the lesion effects of the amygdala, an important neural module in emotional behaviour, on USVs. We recorded USVs from mice in the lesion and the control (sham operation) groups upon presentation of females and compared USVs before and after surgery. We found that the mean syllable duration of the USVs shortened and the appearance rate of longer syllables decreased after the surgery. The main reasons for these alterations could be explained by the altered courtship behaviour. As reported previously, the mounting behaviour of the lesion group after surgery was markedly less than that of the control group. Therefore, the appearance rate of those longer syllables would decrease logically because longer syllables primarily appear during mounting and intromission. However, we can hypothesize another scenario for the alterations to vocal behaviour: effects on the direct amygdala-periaqueductal grey (PAG) projection might be involved in the increase in the appearance rate of shorter syllables owing to lesion-induced loss of emotions, such as vigilance. Overall, the results suggested two possible mechanisms of the amygdala lesions on the alteration of the vocal behaviour.

Hierarchical emergence of sequence sensitivity in the songbird auditory forebrain.

Bengalese finches (Lonchura striata var. domestica) generate more complex sequences in their songs than zebra finches. Because of this, we chose this species to explore the signal processing of sound sequence in the primary auditory forebrain area, field L, and in a secondary area, the caudomedial nidopallium (NCM). We simultaneously recorded activity from multiple single units in urethane-anesthetized birds. We successfully replicated the results of a previous study in awake zebra finches examining stimulus-specific habituation of NCM neurons to conspecific songs. Then, we used an oddball paradigm and compared the neural response to deviant sounds that were presented infrequently, with the response to standard sounds, which were presented frequently. In a single sound oddball task, two different song elements were assigned for the deviant and standard sounds. The response bias to deviant elements was larger in NCM than in field L. In a triplet sequence oddball task, two triplet sequences containing elements ABC and ACB were assigned as the deviant and standard. Only neurons in NCM that displayed broad-shaped spike waveforms had sensitivity to the difference in element order. Our results suggest the hierarchical processing of complex sound sequences in the songbird auditory forebrain.

Functional evidence for internal feedback in the songbird brain nucleus HVC.

The song control system of songbirds consists mainly of the ‘motor pathway’ and ‘anterior forebrain pathway’. The medial magnocellular nucleus of anterior nidopallium (mMAN) projects to the song control nucleus HVC, which is the point of divergence of the two pathways. We made simultaneous multiunit electrophysiological recordings from the mMAN and HVC in anesthetized Bengalese finches. We confirmed that the mMAN neurons showed song-selective auditory responses, and found temporal correlations between song-related activities of the mMAN and HVC neurons. The temporal relationship between the neural activation of the HVC and mMAN suggests that these nuclei are parts of a closed loop, which could provide internal feedback to the HVC for sequential syllable control.

Affective valence of neurons in the vicinity of the rat amygdala: Single unit activity in response to a conditioned behavior and vocal sound playback

Abstract We recorded single unit activity within and around the rat amygdala while rats were engaged in an operant task (which included both reward and aversive trials) and during playback of ultrasonic vocalizations (USVs) to determine if there existed neurons which responded to two different types of either positive contexts (i.e., water reward and positively associated 50 kHz vocalizations) or negative contexts (i.e., white noise and negatively associated 22 kHz vocalizations). Ultimately, we wanted to determine if these two contexts (operant condition task and vocal sounds) could be represented as either positive or negative in a single neuron. Neural activity in 90% of cells was modulated in response to one or more of those events. A small number of those cells showed neural responses to both the aversive operant trials and 22 kHz USVs, but did not show responses to reward operant trials or 50 kHz USVs, suggesting the activity of these neurons encodes for similar negative emotion in response to these two contexts. Some cells showed responses to either the reward trials or 50 kHz USVs, but no cells showed responses to both, suggesting that these cells do not show a common response to events associated with positive emotion. This might mean that 50 kHz vocal sounds and the operant rewards were segregated into two different categories within the neural representation at the level of the amygdala, even though it appeared that both events were associated with positive emotions in rats.

Food rewards modulate the activity of song neurons in Bengalese finches.

Vocal learning, a critical component of speech acquisition, is a rare trait in animals. Songbirds are a well‐established animal model in vocal learning research; male birds acquire novel vocal patterns and have a well‐developed ‘song system’ in the brain. Although this system is unique to songbirds, anatomical and physiological studies have reported similarities between the song system and the thalamo‐cortico‐basal ganglia circuit that is conserved among reptiles, birds, and mammals. Here, we focused on the similarity of the neural response between these two systems while animals were engaging in operant tasks. Neurons in the basal ganglia of vertebrates are activated in response to food rewards and reward predictions in behavioral tasks. A striatal nucleus in the avian song system, Area X, is necessary for vocal learning and is considered specialized for singing. We found that the spiking activity of singing‐related Area X neurons was modulated by food rewards and reward signals in an operant task. As previous studies showed that Area X is not critical for general cognitive tasks, the role of Area X in general learning might be limited and vestigial. However, our results provide a new viewpoint to investigate the independence of the vocal learning system from neural systems involved in other cognitive tasks.

Effects of visual stimulation on the auditory responses of the HVC song control nucleus in anesthetized Bengalese Finches

ABSTRACT In songbirds, the auditory neurons of the telencephalic song control nuclei, especially those in the high vocal center (HVC), respond to the birds own song (BOS) selectively. Since songs are elicited by the sight of conspecific females and interrupted by intense visual stimulation, such as strobe lights, visual input might modulate this auditory selectivity. This study used acute electrophysiological experiments using Bengalese Finches (Lonchura striata var. domestica) to examine whether strobe lights affect this auditory response. The results showed that visual inputs did not affect the neural activities in response to the BOS. When the visual stimulus was presented alone, we did not record comparable neural activities to auditory stimuli, although vague, weak electrical potential fluctuations were observed. This means that direct visual inputs do not reach all HVC neurons that have BOS selectivity, and the effects of visual information might be very limited in the song control system. Although visual information should have some relationship to singing behaviors, such effects might be mediated by indirect connections from the visual system via unidentified emotional modules.

Vocal conditioning with playback of two template sounds in budgerigars

We examined a capability of budgerigars to produce a similar vocal pattern to a sound stimulus presented immediately just before. For this purpose, we trained birds using an operant conditioning procedure. In the training, two types of the birds’ own call were used as the auditory stimuli. Then, they were tested by probe stimuli (another vocal pattern of the subjects’ own, other birds’ vocalization). At test trials, the birds vocalized not any similar sounds in response to the probe stimuli but one of the vocal patterns which was produced at the training trials. Then, we attempted to train the birds to produce vocal patterns following playback sounds which were slightly changing as the trials went. 24-step intermediate sounds between two birds’ own vocal patterns were synthesized. Those intermediate sounds were shifting step-by-step from one to the other at each trial in a single session. Eventually, a bird created some novel sounds which were similar to those intermediate stimuli and had been never produced at the training trials. Taken together, the birds did not use the playback sounds as the vocal reference under the operant procedure. However, birds might store those playback sounds as the potential vocal repertoire.