David H. Reser

Click train encoding in primary auditory cortex of the awake monkey: Evidence for two mechanisms subserving pitch perception

Multiunit activity (MUA) and current source density (CSD) patterns evoked by click trains are examined in primary auditory cortex (A1) of three awake monkeys. Temporal and spectral features of click trains are differentially encoded in A1. Encoding of temporal features occurs at rates of 100-200 Hz through phase-locked activity in the MUA and CSD, is independent of pulse polarity pattern, and occurs in high best frequency (BF) regions of A1. The upper limit of ensemble-wide phase-locking is about 400 Hz in the input to A1, as manifested in the cortical middle laminae CSD and MUA of thalamocortical fibers. In contrast, encoding of spectral features occurs in low BF regions, and resolves both the f0 and harmonics of the stimuli through local maxima of activity determined by the tonotopic organization of the recording sites. High-pass filtered click trains decrease spectral encoding in low BF regions without modifying phase-locked responses in high BF regions. These physiological responses parallel features of human pitch perception for click trains, and support the existence of two distinct physiological mechanisms involved in pitch perception: the first using resolved harmonic components and the second utilizing unresolved harmonics that is based on encoding stimulus waveform periodicity.

Connections of the Dorsomedial Visual Area: Pathways for Early Integration of Dorsal and Ventral Streams in Extrastriate Cortex

The dorsomedial area (DM), a subdivision of extrastriate cortex characterized by heavy myelination and relative emphasis on peripheral vision, remains the least understood of the main targets of striate cortex (V1) projections in primates. Here we placed retrograde tracer injections encompassing the full extent of this area in marmoset monkeys, and performed quantitative analyses of the numerical strengths and laminar patterns of its afferent connections. We found that feedforward projections from V1 and from the second visual area (V2) account for over half of the inputs to DM, and that the vast majority of the remaining connections come from other topographically organized visual cortices. Extrastriate projections to DM originate in approximately equal proportions from adjacent medial occipitoparietal areas, from the superior temporal motion-sensitive complex centered on the middle temporal area (MT), and from ventral stream-associated areas. Feedback from the posterior parietal cortex and other association areas accounts for <10% of the connections. These results do not support the hypothesis that DM is specifically associated with a medial subcircuit of the dorsal stream, important for visuomotor integration. Instead, they suggest an early-stage visual-processing node capable of contributing across cortical streams, much as V1 and V2 do. Thus, although DM may be important for providing visual inputs for guided body movements (which often depend on information contained in peripheral vision), this area is also likely to participate in other functions that require integration across wide expanses of visual space, such as perception of self-motion and contour completion.

Colour processing in complex environments: insights from the visual system of bees

Colour vision enables animals to detect and discriminate differences in chromatic cues independent of brightness. How the bee visual system manages this task is of interest for understanding information processing in miniaturized systems, as well as the relationship between bee pollinators and flowering plants. Bees can quickly discriminate dissimilar colours, but can also slowly learn to discriminate very similar colours, raising the question as to how the visual system can support this, or whether it is simply a learning and memory operation. We discuss the detailed neuroanatomical layout of the brain, identify probable brain areas for colour processing, and suggest that there may be multiple systems in the bee brain that mediate either coarse or fine colour discrimination ability in a manner dependent upon individual experience. These multiple colour pathways have been identified along both functional and anatomical lines in the bee brain, providing us with some insights into how the brain may operate to support complex colour discrimination behaviours.

Tonotopic organization of responses reflecting stop consonant place of articulation in primary auditory cortex (A1) of the monkey

Current source density and multiunit activity elicited by stop consonant-vowel syllables were examined in primary auditory cortex of an awake monkey. Relative amplitudes of the speech-evoked responses were determined by the onset spectra of the consonants and the tonotopic organization. This finding supports the psychoacoustic hypothesis that the onset spectra of stop consonants are important determinants for the discrimination of place of articulation.

Cortical Input to the Frontal Pole of the Marmoset Monkey

We used fluorescent tracers to map the pattern of cortical afferents to frontal area 10 in marmosets. Dense projections originated in several subdivisions of orbitofrontal cortex, in the medial frontal cortex (particularly areas 14 and 32), and in the dorsolateral frontal cortex (particularly areas 8Ad and 9). Major projections also stemmed, in variable proportions depending on location of the injection site, from both the inferior and superior temporal sensory association areas, suggesting a degree of audiovisual convergence. Other temporal projections included the superior temporal polysensory cortex, temporal pole, and parabelt auditory cortex. Medial area 10 received additional projections from retrosplenial, rostral calcarine, and parahippocampal areas, while lateral area 10 received small projections from the ventral somatosensory and premotor areas. There were no afferents from posterior parietal or occipital areas. Most frontal connections were balanced in terms of laminar origin, giving few indications of an anatomical hierarchy. The pattern of frontopolar afferents suggests an interface between high-order representations of the sensory world and internally generated states, including working memory, which may subserve ongoing evaluation of the consequences of decisions as well as other cognitive functions. The results also suggest the existence of functional differences between subregions of area 10.

Pitch vs. spectral encoding of harmonic complex tones in primary auditory cortex of the awake monkey.

Neuromagnetic studies in humans and single-unit studies in monkeys have provided conflicting views regarding the role of primary auditory cortex (A1) in pitch encoding. While the former support a topographic organization based on the pitch of complex tones, single-unit studies support the classical tonotopic organization of A1 defined by the spectral composition of the stimulus. It is unclear whether the incongruity of these findings is due to limitations of noninvasive recordings or whether the discrepancy genuinely reflects pitch representation based on population encoding. To bridge these experimental approaches, we examined neuronal ensemble responses in A1 of the awake monkey using auditory evoked potential (AEP), multiple-unit activity (MUA) and current source density (CSD) techniques. Macaque monkeys can perceive the missing fundamental of harmonic complex tones and therefore serve as suitable animal models for studying neural encoding of pitch. Pure tones and harmonic complex tones missing the fundamental frequency (f0) were presented at 60 dB SPL to the ear contralateral to the hemisphere from which recordings were obtained. Laminar response profiles in A1 reflected the spectral content rather than the pitch (missing f0) of the compound stimuli. These findings are consistent with single-unit data and indicate that the cochleotopic organization is preserved at the level of A1. Thus, it appears that pitch encoding of multi-component sounds is more complex than suggested by noninvasive studies, which are based on the assumption of a single dipole generator within the superior temporal gyrus. These results support a pattern recognition mechanism of pitch encoding based on a topographic representation of stimulus spectral composition at the level of A1.

Complex tone processing in primary auditory cortex of the awake monkey. I. Neural ensemble correlates of roughness

Previous physiological studies [e.g., Bieser and Muller-Preuss, Exp. Brain Res. 108, 273-284 (1996); Schulze and Langner, J. Comp. Physiol. A 181, 651-663 (1997); Steinschneider et al., J. Acoust. Soc. Am. 104, 2935-2955 (1998)] have suggested that neural activity in primary auditory cortex (A1) phase-locked to the waveform envelope of complex sounds with low (<300 Hz) periodicities may represent a neural correlate of roughness perception. However, a correspondence between these temporal response patterns and human psychophysical boundaries of roughness has not yet been demonstrated. The present study examined whether the degree of synchronized phase-locked activity of neuronal ensembles in A1 of the awake monkey evoked by complex tones parallels human psychoacoustic data defining the existence region and frequency dependence of roughness. Stimuli consisted of three consecutive harmonics of fundamental frequencies (f(0)s) ranging from 25 to 4000 Hz. The center frequency of the complex tones was fixed at the best frequency (BF) of the cortical sites, which ranged from 0.3 to 10 kHz. Neural ensemble activity in the thalamorecipient zone (lower lamina III) and supragranular cortical laminae (upper lamina III and lamina II) was measured using multiunit activity and current source density techniques and the degree of phase-locking to the f0 was quantified by spectral analysis. In the thalamorecipient zone, the stimulus f0 at which phase-locking was maximal increased with BF and reached an upper limit between 75 and 150 Hz for BFs greater than about 3 kHz. Estimates of limiting phase-locking rates also increased with BF and approximated psychoacoustic values for the disappearance of roughness. These physiological relationships parallel human perceptual data and therefore support the relevance of phase-locked activity of neuronal ensembles in A1 for the physiological representation of roughness.

Complex tone processing in primary auditory cortex of the awake monkey. II. Pitch versus critical band representation

Noninvasive neurophysiological studies in humans support the existence of an orthogonal spatial representation of pure tone frequency and complex tone pitch in auditory cortex [Langner et al., J. Comp. Physiol. A 181, 665-676 (1997)]. However, since this topographic organization is based on neuromagnetic responses evoked by wideband harmonic complexes (HCs) of variable fundamental frequency (f0), and thus interharmonic frequency separation (deltaF), critical band filtering effects due to differential resolvability of harmonics may have contributed to shaping these responses. To test this hypothesis, the present study examined responses evoked by three-component HCs of variable f0 in primary auditory cortex (A1) of the awake monkey. The center frequency of the HCs was fixed at the best frequency (BF) of the cortical site. Auditory evoked potential (AEP), multiunit activity, and current source density techniques were used to evaluate A1 responses as a function of f0 (=deltaF). Generally, amplitudes of nearly all response components increased with f0, such that maximal responses were evoked by HCs comprised of low-order resolved harmonics. Statistically significant increases in response amplitude typically occurred at deltaFs between 10% and 20% of center frequency, suggestive of critical bandlike behavior. Complex tone response amplitudes also reflected nonlinear summation in that they could not be predicted by the pure tone frequency sensitivity curves of the cortical sites. A mechanism accounting for the observed results is proposed which involves mutual lateral inhibitory interactions between responses evoked by stimulus components lying within the same critical band. As intracortical AEP components likely to be propagated to the scalp were also strongly modulated by deltaF, these findings indicate that noninvasive recordings of responses to complex sounds may require a consideration of critical band effects in their interpretation.

Spatial and temporal frequency tuning in striate cortex: functional uniformity and specializations related to receptive field eccentricity

In light of anatomical evidence suggesting differential connection patterns in central vs. peripheral representations of cortical areas, we investigated the extent to which the response properties of cells in the primary visual area (V1) of the marmoset change as a function of eccentricity. Responses to combinations of the spatial and temporal frequencies of visual stimuli were quantified for neurons with receptive fields ranging from 3° to 70° eccentricity. Optimal spatial frequencies and stimulus speeds reflected the expectation that the responses of cells throughout V1 are essentially uniform, once scaled according to the cortical magnification factor. In addition, temporal frequency tuning was similar throughout V1. However, spatial frequency tuning curves depended both on the cell’s optimal spatial frequency and on the receptive field eccentricity: cells with peripheral receptive fields showed narrower bandwidths than cells with central receptive fields that were sensitive to the same optimal spatial frequency. Although most V1 cells had separable spatial and temporal frequency tuning, the proportion of neurons displaying significant spatiotemporal interactions increased in the representation of far peripheral vision (> 50°). In addition, of the fewer than 5% of V1 cells that showed robust (spatial frequency independent) selectivity to stimulus speed, most were concentrated in the representation of the far periphery. Spatiotemporal interactions in the responses of many cells in the peripheral representation of V1 reduced the ambiguity of responses to high‐speed (> 30°/s) signals. These results support the notion of a relative specialization for motion processing in the far peripheral representations of cortical areas, including V1.

Honeybees (Apis mellifera) Learn Color Discriminations via Differential Conditioning Independent of Long Wavelength (Green) Photoreceptor Modulation

Background Recent studies on colour discrimination suggest that experience is an important factor in how a visual system processes spectral signals. In insects it has been shown that differential conditioning is important for processing fine colour discriminations. However, the visual system of many insects, including the honeybee, has a complex set of neural pathways, in which input from the long wavelength sensitive (‘green’) photoreceptor may be processed either as an independent achromatic signal or as part of a trichromatic opponent-colour system. Thus, a potential confound of colour learning in insects is the possibility that modulation of the ‘green’ photoreceptor could underlie observations. Methodology/Principal Findings We tested honeybee vision using light emitting diodes centered on 414 and 424 nm wavelengths, which limit activation to the short-wavelength-sensitive (‘UV’) and medium-wavelength-sensitive (‘blue’) photoreceptors. The absolute irradiance spectra of stimuli was measured and modelled at both receptor and colour processing levels, and stimuli were then presented to the bees in a Y-maze at a large visual angle (26°), to ensure chromatic processing. Sixteen bees were trained over 50 trials, using either appetitive differential conditioning (N = 8), or aversive-appetitive differential conditioning (N = 8). In both cases the bees slowly learned to discriminate between the target and distractor with significantly better accuracy than would be expected by chance. Control experiments confirmed that changing stimulus intensity in transfers tests does not significantly affect bee performance, and it was possible to replicate previous findings that bees do not learn similar colour stimuli with absolute conditioning. Conclusion Our data indicate that honeybee colour vision can be tuned to relatively small spectral differences, independent of ‘green’ photoreceptor contrast and brightness cues. We thus show that colour vision is at least partly experience dependent, and behavioural plasticity plays an important role in how bees exploit colour information.