Michael Brosch

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.

The cognitive auditory cortex: task-specificity of stimulus representations.

Auditory cortex (AC), like subcortical auditory nuclei, represents properties of auditory stimuli by spatiotemporal activation patterns across neurons. A tacit assumption of AC research has been that the multiplicity of functional maps in primary and secondary areas serves a refined continuation of subcortical stimulus processing, i.e. a parallel orderly analysis of distinct properties of a complex sound. This view, which was mainly derived from exposure to parametric sound variation, may not fully capture the essence of cortical processing. Neocortex, in spite of its parcellation into diverse sensory, motor, associative, and cognitive areas, exhibits a rather stereotyped local architecture. The columnar arrangement of the neocortex and the quantitatively dominant connectivity with numerous other cortical areas are two of its key features. This suggests that cortex has a rather common function which lies beyond those usually leading to the distinction of functional areas. We propose that task-relatedness of the way, how any information can be represented in cortex, is one general consequence of the architecture and corticocortical connectivity. Specifically, this hypothesis predicts different spatiotemporal representations of auditory stimuli when concepts and strategies how these stimuli are analysed do change. We will describe, in an exemplary fashion, cortical patterns of local field potentials in gerbil, of unit spiking activity in monkey, and of fMRI signals in human AC during the execution of different tasks mainly in the realm of category formation of sounds. We demonstrate that the representations reflect context- and memory-related, conceptual and executional aspects of a task and that they can predict the behavioural outcome.

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.

Stimulus-Specific Synchronizations in Cat Visual Cortex: Multiple Microelectrode and Correlation Studies from Several Cortical Areas

It might be imagined that the recently observed synchronizations among neurons of cat visual cortex are epiphenomena or side products of cellular properties with no causal significance for visual signal processing. Our working hypothesis, on the contrary, assumes that synchronization of neural activities forms the basis of a flexible mechanism for feature linking in sensory systems. Specified for the visual system, the hypothesis states that the receptive field properties of visual neurons in different parts ol the visual system can be linked into a perceptual whole by synchronizing the activities of those neurons that are activated by a coherent visual stimulus. We further assume that synchronization among the activities in distributed neural assemblies is internally enhanced or even generated via a specific linking (association) network that connects corresponding and noncorresponding locations of the cortical representations of visual space.

Tone-sequence analysis in the auditory cortex of awake macaque monkeys

The present study analyzed neuronal responses to two-tone sequences in the auditory cortex of three awake macaque monkeys. The monkeys were passively exposed to 430 different two-tone sequences, in which the frequency of the first tone and the interval between the first and the second tone in the sequence were systematically varied. The frequency of the second tone remained constant and was matched to the single-tone frequency sensitivity of the neurons. Multiunit activity was recorded from 109 sites in the primary auditory cortex and posterior auditory belt. We found that the first tone in the sequence could inhibit or facilitate the response to the second tone. Type and magnitude of poststimulatory effects depended on the sequence parameters and were related to the single-tone frequency sensitivity of neurons, similar to previous observations in the auditory cortex of anesthetized animals. This suggests that some anesthetics produce, at the most, moderate changes of poststimulatory inhibition and facilitation in the auditory cortex. Hence many properties of the sequence-sensitivity of neurons in the auditory cortex measured in anesthetized preparations can be applied to neurons in the auditory cortex of awake subjects.

SYNCHRONOUS HIGH-FREQUENCY OSCILLATIONS IN CAT AREA 18

The present study extends knowledge of the basic properties of correlated oscillatory activity patterns in the visual cortex of anaesthetized cats. Recordings with multiple electrodes were performed in area 18 and the correlations of multi‐unit activity in the frequency range 35‐80 Hz were determined using the coherence function. Statistical analysis revealed that the multi‐unit correlations depended on the cortical distance between the recording sites, the orientation selectivity of the neurons and their cortical layer. On average, correlations dropped to chance level within several millimetres and were higher in lower than in upper cortical layers. Similar results were found by analysing the correlations of oscillatory patterns in local field potentials recorded from the same electrodes. Correlations of neurons with similar orientation preferences were higher than those of neurons with different orientation preferences. Comparison to a matched sample from area 17 showed that the correlations in areas 18 and 17 depended on similar properties of the neurons. The dependences of correlated oscillations resembled the known pattern and specificity of intra‐areal fibre connections, suggesting that the correlations were intracortically established. Since correlations were specifically and not randomly related to the response properties of cortical neurons and were prominent in a visual area other than area 17, the findings suggest that correlated oscillatory activity provides a potential neural code supporting sensory information processing.

Neuronal mechanisms of auditory backward recognition masking in macaque auditory cortex

THE sensation of a single sound event can be altered by subsequent sounds. This study searched for neural mechanisms of such retroactive effects in macaque auditory cortex by comparing neural responses to single tones with responses to two consecutive tones. Retroactive influences were found to affect late parts of the response to a tone, which comprised 53/134 of the recordings of action potentials and 88/131 of the recordings of field potentials performed in primary, caudal, and medial auditory fields. If before or during the occurrence of the late response to the first tone a second tone was presented the late response was suppressed. Suppression of late cortical responses parallels perceptual phenomena like backward recognition masking, suggesting that suppression of late responses provides a neural correlate of auditory backward effects.

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.