Cortical Activation Patterns Evoked by Temporally Asymmetric Sounds and Their Modulation by Learning.

When complex sounds are reversed in time, the original and reversed versions are perceived differently in spectral and temporal dimensions despite their identical duration and long-term spectrum-power profiles. Spatiotemporal activation patterns evoked by temporally asymmetric sound pairs demonstrate how the temporal envelope determines the readout of the spectrum. We examined the patterns of activation evoked by a temporally asymmetric sound pair in the primary auditory field (AI) of anesthetized guinea pigs and determined how discrimination training modified these patterns. Optical imaging using a voltage-sensitive dye revealed that a forward ramped-down natural sound (F) consistently evoked much stronger responses than its time-reversed, ramped-up counterpart (revF). The spatiotemporal maximum peak (maxP) of F-evoked activation was always greater than that of revF-evoked activation, and these maxPs were significantly separated within the AI. Although discrimination training did not affect the absolute magnitude of these maxPs, the revF-to-F ratio of the activation peaks calculated at the location where hemispheres were maximally activated (i.e., F-evoked maxP) was significantly smaller in the trained group. The F-evoked activation propagated across the AI along the temporal axis to the ventroanterior belt field (VA), with the local activation peak within the VA being significantly larger in the trained than in the naïve group. These results suggest that the innate network is more responsive to natural sounds of ramped-down envelopes than their time-reversed, unnatural sounds. The VA belt field activation might play an important role in emotional learning of sounds through its connections with amygdala.

Auditory-visual integration in fields of the auditory cortex.

While multimodal interactions have been known to exist in the early sensory cortices, the response properties and spatiotemporal organization of these interactions are poorly understood. To elucidate the characteristics of multimodal sensory interactions in the cerebral cortex, neuronal responses to visual stimuli with or without auditory stimuli were investigated in core and belt fields of guinea pig auditory cortex using real-time optical imaging with a voltage-sensitive dye. On average, visual responses consisted of short excitation followed by long inhibition. Although visual responses were observed in core and belt fields, there were regional and temporal differences in responses. The most salient visual responses were observed in the caudal belt fields, especially posterior (P) and dorsocaudal belt (DCB) fields. Visual responses emerged first in fields P and DCB and then spread rostroventrally to core and ventrocaudal belt (VCB) fields. Absolute values of positive and negative peak amplitudes of visual responses were both larger in fields P and DCB than in core and VCB fields. When combined visual and auditory stimuli were applied, fields P and DCB were more inhibited than core and VCB fields beginning approximately 110 ms after stimuli. Correspondingly, differences between responses to auditory stimuli alone and combined audiovisual stimuli became larger in fields P and DCB than in core and VCB fields after approximately 110 ms after stimuli. These data indicate that visual influences are most salient in fields P and DCB, which manifest mainly as inhibition, and that they enhance differences in auditory responses among fields.

[Information Processing in the Auditory Ventral Stream].

The auditory cortex in humans comprises multiple auditory fields organized hierarchically, similar to that in non-human primates. The ventral auditory stream of the macaque consists of several subdivisions on the supratemporal plane (STP) and the superior temporal gyrus (STG). There are two main axes (caudorostral and mediolateral) for processing auditory information in the STP and STG. Here, we review the neural basis of the integration of spectral and temporal auditory information along the two axes of the ventral auditory stream in the macaque.

Recognition of Modified Conditioning Sounds by Competitively Trained Guinea Pigs.

The guinea pig (GP) is an often-used species in hearing research. However, behavioral studies are rare, especially in the context of sound recognition, because of difficulties in training these animals. We examined sound recognition in a social competitive setting in order to examine whether this setting could be used as an easy model. Two starved GPs were placed in the same training arena and compelled to compete for food after hearing a conditioning sound (CS), which was a repeat of almost identical sound segments. Through a 2-week intensive training, animals were trained to demonstrate a set of distinct behaviors solely to the CS. Then, each of them was subjected to generalization tests for recognition of sounds that had been modified from the CS in spectral, fine temporal and tempo (i.e., intersegment interval, ISI) dimensions. Results showed that they discriminated between the CS and band-rejected test sounds but had no preference for a particular frequency range for the recognition. In contrast, sounds modified in the fine temporal domain were largely perceived to be in the same category as the CS, except for the test sound generated by fully reversing the CS in time. Animals also discriminated sounds played at different tempos. Test sounds with ISIs shorter than that of the multi-segment CS were discriminated from the CS, while test sounds with ISIs longer than that of the CS segments were not. For the shorter ISIs, most animals initiated apparently positive food-access behavior as they did in response to the CS, but discontinued it during the sound-on period probably because of later recognition of tempo. Interestingly, the population range and mean of the delay time before animals initiated the food-access behavior were very similar among different ISI test sounds. This study, for the first time, demonstrates a wide aspect of sound discrimination abilities of the GP and will provide a way to examine tempo perception mechanisms using this animal species.

Neural response to movement of the hand and mouth in the secondary somatosensory cortex of Japanese monkeys during a simple feeding task.

Neural activity was recorded in the secondary somatosensory cortex (SII) of macaque monkeys during a simple feeding task. Around the border between the representations of the hand and face in SII, we found neurons that became active during both retrieving with the hand and eating; 59% had receptive fields (RFs) in the hand/face and the remaining 41% had no RFs. Neurons that responded to touching objects were rarely found. This suggests their sensorimotor function rather than tactile object recognition.

Recognition of non-harmonic natural sounds by small mammals using competitive training.

Animals recognize biologically relevant sounds, such as the non-harmonic sounds made by some predators, and respond with adaptive behaviors, such as escaping. To clarify which acoustic parameters are used for identifying non-harmonic, noise-like, broadband sounds, guinea pigs were conditioned to a natural target sound by introducing a novel training procedure in which 2 or 3 guinea pigs in a group competed for food. A set of distinct behavioral reactions was reliably induced almost exclusively to the target sound in a 2-week operant training. When fully conditioned, individual animals were separately tested for recognition of a set of target-like sounds that had been modified from the target sound, with spectral ranges eliminated or with fine or coarse temporal structures altered. The results show that guinea pigs are able to identify the noise-like non-harmonic natural sounds by relying on gross spectral compositions and/or fine temporal structures, just as birds are thought to do in the recognition of harmonic birdsongs. These findings are discussed with regard to similarities and dissimilarities to harmonic sound recognition. The results suggest that similar but not identical processing that requires different time scales might be used to recognize harmonic and non-harmonic sounds, at least in small mammals.

Interplay of excitation and inhibition elicited by tonal stimulation in pyramidal neurons of primary auditory cortex.

Tonal responses of neurons in the primary auditory cortex are a function of frequency, intensity and ear of stimulation. These responses occasionally display suppression. This review discusses how excitatory and inhibitory synaptic inputs interact to form suppressive responses and how changes in stimulus attributes affect the magnitude and timing of those responses. Stimulation at the characteristic frequency evokes a stereotyped sequence of depolarization (excitatory) and then hyperpolarization (inhibitory), as predicted from the canonical circuitry. Some neurons stimulated at higher sound intensities display a prominent increase in the magnitude of hyperpolarization or a decrease in its latency, both enabling counteraction with the preceding excitation. These interactions, in part, underlie the non-monotonic suppression. Furthermore, monaural non-dominant ear stimulation elicits such a powerful hyperpolarization as to cancel out the depolarization elicited at dominant ear stimulation, suggesting a linear mechanism for the binaural suppression. Alternatively, it elicits a depolarization almost equal in magnitude and time course to that elicited at binaural stimulation, suggesting a nonlinear interaction responsible for the suppression. Laminar differences are also noted for these inhibitory interactions.

Triadic synaptic interactions of large corticothalamic terminals in non-lemniscal thalamic nuclei of the cat auditory system.

Large corticothalamic (CT) terminals, presumed to originate from cortical layer 5 pyramidal cells, are distributed predominantly in non-specific thalamic nuclei in mammals. In the auditory system, little is known about whether these CT projections participate in the synaptic aggregation referred to as the triad. We studied synaptic interactions of these terminals with neuronal elements in one of the auditory non-lemniscal thalamic nuclei, the dorsal nucleus of the medial geniculate complex (MGC), in cats. After injections of an anterograde tracer in the primary auditory cortex, areas containing labeled large terminals were examined using an electron microscope. It was revealed that a fraction of large CT terminals participated in complicated synaptic arrangements: labeled terminals making synaptic contacts with vesicle-free dendrites, probably of thalamic principal neurons, and/or vesicle-filled neuronal profiles, probably of presynaptic dendrites (PSDs) of interneurons. In reconstructions or even in single sections, we found that these synaptic connections participated in triadic arrangements. Thus, PSDs postsynaptic to the labeled CT terminals were in turn presynaptic to the vesicle-free dendrites.

Adaptive changes in firing of primary auditory cortical neurons following illumination shift from light to dark in freely moving guinea pigs.

Some animals are forced to rely more on non-visual signals, such as audition or olfaction, than on vision when a bright environment becomes dark. By recording from a primary-like auditory cortex (field A) in freely moving guinea pigs, possible changes in the responsiveness of single units were explored in association with illumination changes. For a subset of units, we found that robust decreases (off-decrease) or increases (off-increase) in baseline discharge (BsD) were initiated soon after room light was silently extinguished. These neuronal changes were accompanied by the initiation of explorative locomotion, possibly reflecting a changed internal brain state. Preferred acoustic stimuli evoked salient excitatory responses against the reduced BsD level in the dark for the off-decrease units, and salient inhibitory responses against the increased BsD level for the off-increase units. Histological verification indicated that the units showing such BsD changes were located predominantly in layer V or its vicinity. These results are discussed in the context of the effects of the brainstem neuromodulatory systems that are activated during behavioral adaptation to new environments.

Extension of corticocortical afferents into the anterior bank of the intraparietal sulcus by tool-use training in adult monkeys.

When humans use a tool, it becomes an extension of the hand physically and perceptually. Common introspection might occur in monkeys trained in tool-use, which should depend on brain operations that constantly update and automatically integrate information about the current intrinsic (somatosensory) and the extrinsic (visual) status of the body parts and the tools. The parietal cortex plays an important role in using tools. Intraparietal neurones of naïve monkeys mostly respond unimodally to somatosensory stimuli; however, after training these neurones become bimodally active and respond to visual stimuli. The response properties of these neurones change to code the body images modified by assimilation of the tool to the hand holding it. In this study, we compared the projection patterns between visually related areas and the intraparietal cortex in trained and naïve monkeys using tracer techniques. Light microscopy analyses revealed the emergence of novel projections from the higher visual centres in the vicinity of the temporo-parietal junction and the ventrolateral prefrontal areas to the intraparietal area in monkeys trained in tool-use, but not in naïve monkeys. Functionally active synapses of intracortical afferents arising from higher visual centres to the intraparietal cortex of the trained monkeys were confirmed by electron microscopy. These results provide the first concrete evidence for the induction of novel neural connections in the adult monkey cerebral cortex, which accompanies a process of demanding behaviour in these animals.

Multisensory convergence in calcarine visual areas in macaque monkey.

The neural substrates of multisensory perception and integration are still obscure, especially at the cortical level. Alternative viewpoints emphasize (1) 'bottom-up' processes, where different modalities converge in higher order multisensory areas, or (2) 'top-down' projections from multimodal to unimodal areas. In this anatomic study, we use anterograde tracer injections in parietal (8 monkeys) and auditory (3 monkeys) association areas, and demonstrate direct projections to areas V1 and V2 in the calcarine fissure (i.e. the peripheral visual field representation). The laminar signature, with terminations in layers 1 and/or 6, could be consistent with feedback-type connections. A subset of connections from parietal areas, however, branch to both V1 and a ventral extrastriate area (TEO or TEp). Thus, the direct connections to early visual areas V1 and V2 may well operate in conjunction with polysynaptic pathways in a densely parallel network.

Intracellular characterization of suppressive responses in supragranular pyramidal neurons of cat primary auditory cortex in vivo.

Several suppressive processes shape the response properties of auditory neurons, namely lateral inhibition, non-monotonic rate level function and excitation/inhibition binaural interaction. By combining intracellular recording from and staining of layers 2 and 3 pyramidal neurons (PNs) in cat primary auditory cortex, we demonstrate the temporal aspects of depolarization and hyperpolarization underlying these suppressions using pure tone stimulation. Two populations can be distinguished by the occurrence of hyperpolarization following onset depolarization (O-DEP). In layer 2 PNs there is an absence of hyperpolarization following O-DEP, while in layer 3 PNs hyperpolarization follows O-DEP. The latency of O-DEP is shortest at the neuron's best frequency. The latency shortens as sound intensity increases. In non-monotonic PNs, hyperpolarization onset becomes shorter as sound intensity increases. This earlier onset of hyperpolarization shortens the duration of the preceding O-DEP, resulting in a decreased O-DEP amplitude. Diverse patterns in the temporal interaction of depolarization and hyperpolarization underlie the binaural suppression interaction. These results demonstrate that diverse suppressive responses result from differences in the temporal timing of excitation and inhibition. The present results also suggest the possibility of distinct connections between PNs responding in a similar manner.