Elena Selezneva

Nonauditory Events of a Behavioral Procedure Activate Auditory Cortex of Highly Trained Monkeys

A central tenet in brain research is that early sensory cortex is modality specific, and, only in exceptional cases, such as deaf and blind subjects or professional musicians, is influenced by other modalities. Here we describe extensive cross-modal activation in the auditory cortex of two monkeys while they performed a demanding auditory categorization task: after a cue light was turned on, monkeys could initiate a tone sequence by touching a bar and then earn a reward by releasing the bar on occurrence of a falling frequency contour in the sequence. In their primary auditory cortex and posterior belt areas, we found many acoustically responsive neurons whose firing was synchronized to the cue light or to the touch or release of the bar. Of 315 multiunits, 45 exhibited cue light-related firing, 194 exhibited firing that was related to bar touch, and 268 exhibited firing that was related to bar release. Among 60 single units, we found one neuron with cue light-related firing, 21 with bar touch-related firing, and 36 with release-related firing. This firing disappeared at individual sites when the monkeys performed a visual detection task. Our findings corroborate and extend recent findings on cross-modal activation in the auditory cortex and suggests that the auditory cortex can be activated by visual and somatosensory stimulation and by movements. We speculate that the multimodal corepresentation in the auditory cortex has arisen from the intensive practice of the subjects with the behavioral procedure and that it facilitates the performance of audiomotor tasks in proficient subjects.

Dual Time Scales for Categorical Decision Making in Auditory Cortex

Category formation allows us to group perceptual objects into meaningful classes and is fundamental to cognition. Categories can be derived from similarity relationships of object features by using prototypes or multiple exemplars, or from abstract relationships of features and rules . A variety of brain areas have been implicated in categorization processes, but mechanistic insights on the single-cell and local-network level are still rare and limited to the matching of individual objects to categories . For directional categorization of tone steps, as in melody recognition , abstract relationships between sequential events (higher or lower in frequency) have to be formed. To explore the neuronal mechanisms of this categorical identification of step direction, we trained monkeys for more than two years on a contour-discrimination task with multiple tone sequences. In the auditory cortex of these highly trained monkeys, we identified two interrelated types of neuronal firing: Increased phasic responses to tones categorically represented the reward-predicting downward frequency steps and not upward steps; subsequently, slow modulations of tonic firing predicted the behavioral decisions of the monkeys, including errors. Our results on neuronal mechanisms of categorical stimulus identification and of decision making attribute a cognitive role to auditory cortex, in addition to its role in signal processing.

Representation of reward feedback in primate auditory cortex

It is well established that auditory cortex is plastic on different time scales and that this plasticity is driven by the reinforcement that is used to motivate subjects to learn or to perform an auditory task. Motivated by these findings, we study in detail properties of neuronal firing in auditory cortex that is related to reward feedback. We recorded from the auditory cortex of two monkeys while they were performing an auditory categorization task. Monkeys listened to a sequence of tones and had to signal when the frequency of adjacent tones stepped in downward direction, irrespective of the tone frequency and step size. Correct identifications were rewarded with either a large or a small amount of water. The size of reward depended on the monkeys’ performance in the previous trial: it was large after a correct trial and small after an incorrect trial. The rewards served to maintain task performance. During task performance we found three successive periods of neuronal firing in auditory cortex that reflected (1) the reward expectancy for each trial, (2) the reward-size received, and (3) the mismatch between the expected and delivered reward. These results, together with control experiments suggest that auditory cortex receives reward feedback that could be used to adapt auditory cortex to task requirements. Additionally, the results presented here extend previous observations of non-auditory roles of auditory cortex and shows that auditory cortex is even more cognitively influenced than lately recognized.

Macaque monkeys discriminate pitch relationships

This study demonstrates that non-human primates can categorize the direction of the pitch change of tones in a sequence. Two Macaca fascicularis were trained in a positive-reinforcement behavioral paradigm in which they listened to sequences of a variable number of different acoustic items. The training of discriminating pitch direction was divided into three phases with increasing task complexity. In the first two phases, subjects learned to employ a same/different rule. In phase 1, they discriminated acoustic items of different sound quality. Subjects had to respond when there was a change from repeating noise bursts to repeating click trains or vice versa. In phase II, acoustic items differed along one physical dimension only. Subjects had to respond to a change of the frequency of a repeating series of pure tones. In phase III, sequences consisted of three series of repeating tones of different frequency. Subjects were required to respond when the frequency of the tones changed in a downward direction and to refrain from responding when the frequency remained constant or increased. After several ten thousand trials, subjects categorized pitch direction well above chance level. The discrimination was performed over a 4.5-octave range of frequencies and was largely independent of the temporal and ordinal position of the downward pitch direction within the sequence. These results demonstrate that monkeys can recognize pitch relationships and thus that monkeys have the concept of ordinal relations between acoustic items.

Formation of associations in auditory cortex by slow changes of tonic firing

We review event-related slow firing changes in the auditory cortex and related brain structures. Two types of changes can be distinguished, namely increases and decreases of firing, lasting in the order of seconds. Triggering events can be auditory stimuli, reinforcers, and behavioral responses. Slow firing changes terminate with reinforcers and possibly with auditory stimuli and behavioral responses. A necessary condition for the emergence of slow firing changes seems to be that subjects have learnt that consecutive sensory or behavioral events are contingent on reinforcement. They disappear when the contingencies are no longer present. Slow firing changes in auditory cortex bear similarities with slow changes of neuronal activity that have been observed in subcortical parts of the auditory system and in other non-sensory brain structures. We propose that slow firing changes in auditory cortex provide a neuronal mechanism for anticipating, memorizing, and associating events that are related to hearing and of behavioral relevance. This may complement the representation of the timing and types of auditory and auditory-related events which may be provided by phasic responses in auditory cortex. The presence of slow firing changes indicates that many more auditory-related aspects of a behavioral procedure are reflected in the neuronal activity of auditory cortex than previously assumed.

A multilevel and cross-modal approach towards neuronal mechanisms of auditory streaming.

We report first results of a multilevel, cross-modal study on the neuronal mechanisms underlying auditory sequential streaming, with the focus on the impact of visual sequences on perceptually ambiguous tone sequences which can either be perceived as two separate streams or one alternating stream. We combined two psychophysical experiments performed on humans and monkeys with two human brain imaging experiments which allow to obtain complementary information on brain activation with high spatial (fMRI) and high temporal (MEG) resolution. The same acoustic paradigm based on the pairing of tone sequences with visual stimuli was used in all human studies and, in an adapted version, in the psychophysical study on monkeys. Our multilevel approach provides experimental evidence that the pairing of auditory and visual stimuli can reliably introduce a bias towards either an integrated or a segregated perception of ambiguous sequences. Thus, comparable to an explicit instruction, this approach can be used to control the subjects perceptual organization of an ambiguous sound sequence without the need for the subject to directly report it. This finding is of particular importance for animal studies because it allows to compare electrophysiological responses of auditory cortex neurons to the same acoustic stimulus sequence eliciting either a segregated or integrated percept.

Rhythm sensitivity in macaque monkeys

This study provides evidence that monkeys are rhythm sensitive. We composed isochronous tone sequences consisting of repeating triplets of two short tones and one long tone which humans perceive as repeating triplets of two weak and one strong beat. This regular sequence was compared to an irregular sequence with the same number of randomly arranged short and long tones with no such beat structure. To search for indication of rhythm sensitivity we employed an oddball paradigm in which occasional duration deviants were introduced in the sequences. In a pilot study on humans we showed that subjects more easily detected these deviants when they occurred in a regular sequence. In the monkeys we searched for spontaneous behaviors the animals executed concomitant with the deviants. We found that monkeys more frequently exhibited changes of gaze and facial expressions to the deviants when they occurred in the regular sequence compared to the irregular sequence. In addition we recorded neuronal firing and local field potentials from 175 sites of the primary auditory cortex during sequence presentation. We found that both types of neuronal signals differentiated regular from irregular sequences. Both signals were stronger in regular sequences and occurred after the onset of the long tones, i.e., at the position of the strong beat. Local field potential responses were also significantly larger for the durational deviants in regular sequences, yet in a later time window. We speculate that these temporal pattern-selective mechanisms with a focus on strong beats and their deviants underlie the perception of rhythm in the chosen sequences.

Neuronal activity in primate auditory cortex during the performance of audiovisual tasks

This study aimed at a deeper understanding of which cognitive and motivational aspects of tasks affect auditory cortical activity. To this end we trained two macaque monkeys to perform two different tasks on the same audiovisual stimulus and to do this with two different sizes of water rewards. The monkeys had to touch a bar after a tone had been turned on together with an LED, and to hold the bar until either the tone (auditory task) or the LED (visual task) was turned off. In 399 multiunits recorded from core fields of auditory cortex we confirmed that during task engagement neurons responded to auditory and non‐auditory stimuli that were task‐relevant, such as light and water. We also confirmed that firing rates slowly increased or decreased for several seconds during various phases of the tasks. Responses to non‐auditory stimuli and slow firing changes were observed during both the auditory and the visual task, with some differences between them. There was also a weak task‐dependent modulation of the responses to auditory stimuli. In contrast to these cognitive aspects, motivational aspects of the tasks were not reflected in the firing, except during delivery of the water reward. In conclusion, the present study supports our previous proposal that there are two response types in the auditory cortex that represent the timing and the type of auditory and non‐auditory elements of a auditory tasks as well the association between elements.

Reaction times reflect subjective auditory perception of tone sequences in macaque monkeys

Perceptually ambiguous stimuli are useful for testing psychological and neuronal models of perceptual organization, e.g. for studying brain processes that underlie sequential segregation and integration. This is because the same stimuli may give rise to different subjective experiences. For humans, a tone sequence that alternates between a low-frequency and a high-frequency tone is perceptually bistable, and can be perceived as one or two streams. In the current study we present a new method based on response times (RTs) which allows identification ambiguous and unambiguous stimuli for subjects who cannot verbally report their subjective experience. We required two macaque monkeys (macaca fascicularis) to detect the termination of a sequence of light flashes which were either presented alone, or synchronized in different ways with a sequence of alternating low and high tones. We found that the monkeys responded faster to the termination of the flash sequence when the tone sequence terminated shortly before the flash sequence and thus predicted the termination of the flash sequence. This RT gain depended on the frequency separation of the tones. RT gains were largest when the frequency separation was small and the tones were presumably heard mainly as one stream. RT gains were smallest when the frequency separation was large and the tones were presumably mainly heard as two streams. RT gain was of intermediate size for intermediate frequency separations. Similar results were obtained from human subjects. We conclude that the observed RT gains reflect the perceptual organization of the tone sequence, and that tone sequences with an intermediate frequency separation, as for humans, are perceptually ambiguous for monkeys.

Category-specific neuronal activity in left and right auditory cortex and in medial geniculate body of monkeys

We address the question of whether the auditory cortex of the left and right hemisphere and the auditory thalamus are differently involved in the performance of cognitive tasks. To understand these differences on the level of single neurons we compared neuronal firing in the primary and posterior auditory cortex of the two hemispheres and in the medial geniculate body in monkeys while subjects categorized pitch relationships in tone sequences. In contrast to earlier findings in imaging studies performed on humans, we found little difference between the three brain regions in terms of the category-specificity of their neuronal responses, of tonic firing related to task components, and of decision-related firing. The differences between the results in humans and monkeys may result from the type of neuronal activity considered and how it was analyzed, from the auditory cortical fields studied, or from fundamental differences between these species.