Faculty Bibliography

Inhibition plays an essential role in shaping and refining the brain's representation of sensory stimulus attributes. In primary auditory cortex (A1), so-called "sideband" inhibition helps to sharpen the tuning of local neuronal responses. Several distinct types of anatomical circuitry could underlie sideband inhibition, including direct thalamocortical (TC) afferents, as well as indirect intracortical mechanisms. The goal of the present study was to characterize sideband inhibition in A1 and to determine its mechanism by analyzing laminar profiles of neuronal ensemble activity. Our results indicate that both lemniscal and nonlemniscal TC afferents play a role in inhibitory responses via feedforward inhibition and oscillatory phase reset, respectively. We propose that the dynamic modulation of excitability in A1 due to the phase reset of ongoing oscillations may alter the tuning of local neuronal ensembles and can be regarded as a flexible overlay on the more obligatory system of lemniscal feedforward type responses.

Studies in humans and monkeys report widespread multisensory interactions at or near primary visual and auditory areas of neocortex. The range and scale of these effects has prompted increased interest in interconnectivity between the putatively "unisensory" cortices at lower hierarchical levels. Recent anatomical tract-tracing studies have revealed direct projections from auditory cortex to primary visual area (V1) and secondary visual area (V2) that could serve as a substrate for auditory influences over low-level visual processing. To better understand the significance of these connections, we looked for reciprocal projections from visual cortex to caudal auditory cortical areas in macaque monkeys. We found direct projections from area prostriata and the peripheral visual representations of area V2. Projections were more abundant after injections of temporoparietal area and caudal parabelt than after injections of caudal medial belt and the contiguous areas near the fundus of the lateral sulcus. Only one injection was confined to primary auditory cortex (area A1) and did not demonstrate visual connections. The projections from visual areas originated mainly from infragranular layers, suggestive of a "feedback"-type projection. The selective localization of these connections to peripheral visual areas and caudal auditory cortex suggests that they are involved in spatial localization.

Sensory processing is often regarded as a passive process in which biological receptors like photoreceptors and mechanoreceptors transduce physical energy into a neural code. Recent findings, however, suggest that: first, most sensory processing is active, and largely determined by motor/attentional sampling routines; second, owing to rhythmicity in the motor routine, as well as to its entrainment of ambient rhythms in sensory regions, sensory inflow tends to be rhythmic; third, attentional manipulation of rhythms in sensory pathways is instrumental to perceptual selection. These observations outline the essentials of an Active Sensing paradigm, and argue for increased emphasis on the study of sensory processes as specific to the dynamic motor/attentional context in which inputs are acquired

Attending to a stimulus enhances its neuronal representation, even at the level of primary sensory cortex. Cross-modal modulation can similarly enhance a neuronal representation, and this process can also operate at the primary cortical level. Phase reset of ongoing neuronal oscillatory activity has been shown to be an important element of the underlying modulation of local cortical excitability in both cases. We investigated the influence of attention on oscillatory phase reset in primary auditory and visual cortices of macaques performing an intermodal selective attention task. In addition to responses 'driven' by preferred modality stimuli, we noted that both preferred and nonpreferred modality stimuli could 'modulate' local cortical excitability by phase reset of ongoing oscillatory activity, and that this effect was linked to their being attended. These findings outline a supramodal mechanism by which attention can control neurophysiological context, thus determining the representation of specific sensory content in primary sensory cortex

The idea that gamma enhancement reflects a state of high neuronal excitability and synchrony, critical for active brain operations, sets gamma up as a "master" or executor process that determines whether an input is effectively integrated and an effective output is generated. However, gamma amplitude is often coupled to the phase of lower frequency delta or theta oscillations, which would make gamma a "slave" to lower frequency activity. Gamma enslavement is productive and typical during rhythmic mode brain operations; when a predictable rhythm is in play, low and mid-frequency oscillations can be entrained and their excitability fluctuations of put to work in sensory and motor functions. When there is no task relevant rhythm that the system can entrain to, low frequency oscillations become detrimental to processing. Then, a continuous (vigilance) mode of operation is implemented; the system's sensitivity is maximized by suppressing lower frequency oscillations and exploiting continuous gamma band oscillations. Each mode has costs and benefits, and the brain shifts dynamically between them in accord with task demands.

Neuroelectric oscillations reflect rhythmic shifting of neuronal ensembles between high and low excitability states. In natural settings, important stimuli often occur in rhythmic streams, and when oscillations entrain to an input rhythm their high excitability phases coincide with events in the stream, effectively amplifying neuronal input responses. When operating in a 'rhythmic mode', attention can use these differential excitability states as a mechanism of selection by simply enforcing oscillatory entrainment to a task-relevant input stream. When there is no low-frequency rhythm that oscillations can entrain to, attention operates in a 'continuous mode', characterized by extended increase in gamma synchrony. We review the evidence for early sensory selection by oscillatory phase-amplitude modulations, its mechanisms and its perceptual and behavioral consequences.

Whereas gamma-band neuronal oscillations clearly appear integral to visual attention, the role of lower-frequency oscillations is still being debated. Mounting evidence indicates that a key functional property of these oscillations is the rhythmic shifting of excitability in local neuronal ensembles. Here, we show that when attended stimuli are in a rhythmic stream, delta-band oscillations in the primary visual cortex entrain to the rhythm of the stream, resulting in increased response gain for task-relevant events and decreased reaction times. Because of hierarchical cross-frequency coupling, delta phase also determines momentary power in higher-frequency activity. These instrumental functions of low-frequency oscillations support a conceptual framework that integrates numerous earlier findings.

It is widely recognized that viewing a speaker's face enhances vocal communication, although the neural substrates of this phenomenon remain unknown. We propose that the enhancement effect uses the ongoing oscillatory activity of local neuronal ensembles in the primary auditory cortex. Neuronal oscillations reflect rhythmic shifting of neuronal ensembles between high and low excitability states. Our hypothesis holds that oscillations are 'predictively' modulated by visual input, so that related auditory input arrives during a high excitability phase and is thus amplified. We discuss the anatomical substrates and key timing parameters that enable and constrain this effect. Our hypothesis makes testable predictions for future studies and emphasizes the idea that 'background' oscillatory activity is instrumental to cortical sensory processing.

Primates actively examine the visual world by rapidly shifting gaze (fixation) over the elements in a scene. Despite this fact, we typically study vision by presenting stimuli with gaze held constant. To better understand the dynamics of natural vision, we examined how the onset of visual fixation affects ongoing neuronal activity in the absence of visual stimulation. We used multiunit activity and current source density measurements to index neuronal firing patterns and underlying synaptic processes in macaque V1. Initial averaging of neural activity synchronized to the onset of fixation suggested that a brief period of cortical excitation follows each fixation. Subsequent single-trial analyses revealed that 1) neuronal oscillation phase transits from random to a highly organized state just after the fixation onset, 2) this phase concentration is accompanied by increased spectral power in several frequency bands, and 3) visual response amplitude is enhanced at the specific oscillatory phase associated with fixation. We hypothesize that nonvisual inputs are used by the brain to increase cortical excitability at fixation onset, thus "priming" the system for new visual inputs generated at fixation. Despite remaining mechanistic questions, it appears that analysis of fixation-related responses may be useful in studying natural vision.

We measured the timing, areal distribution, and laminar profile of fast, wavelength-insensitive and slower, wavelength-sensitive responses in V1 and extrastriate areas, using laminar current-source density analysis in awake macaque monkeys. There were 3 main findings. 1) We confirmed previously reported significant ventral-dorsal stream latency lags at the level of V4 (V4 mean = 38.7 ms vs. middle temporal mean = 26.9 ms) and inferotemporal cortex (IT mean = 43.4 ms vs. dorsal bank of the superior temporal sulcus mean = 33.9 ms). 2) We found that wavelength-sensitive inputs in areas V1, V4, and IT lagged the wavelength-insensitive responses by significant margins; this lag increased over successive levels of the system. 3) We found that laminar activation profiles in V4 and IT were inconsistent with 'feedforward' input through the ascending ventral cortical pathway; the likely alternative input routes include both lateral inputs from the dorsal stream and direct inputs from nonspecific thalamic neurons. These findings support a 'Framing' Model of ventral stream visual processing in which rapidly conducted inputs, mediated by one or more accessory pathways, modulate the processing of more slowly conducted feedforward inputs