An Attention-Sensitive Memory Trace in Macaque MT Following Saccadic Eye Movements.

We experience a visually stable world despite frequent retinal image displacements induced by eye, head, and body movements. The neural mechanisms underlying this remain unclear. One mechanism that may contribute is transsaccadic remapping, in which the responses of some neurons in various attentional, oculomotor, and visual brain areas appear to anticipate the consequences of saccades. The functional role of transsaccadic remapping is actively debated, and many of its key properties remain unknown. Here, recording from two monkeys trained to make a saccade while directing attention to one of two spatial locations, we show that neurons in the middle temporal area (MT), a key locus in the motion-processing pathway of humans and macaques, show a form of transsaccadic remapping called a memory trace. The memory trace in MT neurons is enhanced by the allocation of top-down spatial attention. Our data provide the first demonstration, to our knowledge, of the influence of top-down attention on the memory trace anywhere in the brain. We find evidence only for a small and transient effect of motion direction on the memory trace (and in only one of two monkeys), arguing against a role for MT in the theoretically critical yet empirically contentious phenomenon of spatiotopic feature-comparison and adaptation transfer across saccades. Our data support the hypothesis that transsaccadic remapping represents the shift of attentional pointers in a retinotopic map, so that relevant locations can be tracked and rapidly processed across saccades. Our results resolve important issues concerning the perisaccadic representation of visual stimuli in the dorsal stream and demonstrate a significant role for top-down attention in modulating this representation.

Spatial Attention Reduces Burstiness in Macaque Visual Cortical Area MST.

Visual attention modulates the firing rate of neurons in many primate cortical areas. In V4, a cortical area in the ventral visual pathway, spatial attention has also been shown to reduce the tendency of neurons to fire closely separated spikes (burstiness). A recent model proposes that a single mechanism accounts for both the firing rate enhancement and the burstiness reduction in V4, but this has not been empirically tested. It is also unclear if the burstiness reduction by spatial attention is found in other visual areas and for other attentional types. We therefore recorded from single neurons in the medial superior temporal area (MST), a key motion-processing area along the dorsal visual pathway, of two rhesus monkeys while they performed a task engaging both spatial and feature-based attention. We show that in MST, spatial attention is associated with a clear reduction in burstiness that is independent of the concurrent enhancement of firing rate. In contrast, feature-based attention enhances firing rate but is not associated with a significant reduction in burstiness. These results establish burstiness reduction as a widespread effect of spatial attention. They also suggest that in contrast to the recently proposed model, the effects of spatial attention on burstiness and firing rate emerge from different mechanisms.

An Extended Normalization Model of Attention Accounts for Feature-Based Attentional Enhancement of Both Response and Coherence Gain.

Paying attention to a sensory feature improves its perception and impairs that of others. Recent work has shown that a Normalization Model of Attention (NMoA) can account for a wide range of physiological findings and the influence of different attentional manipulations on visual performance. A key prediction of the NMoA is that attention to a visual feature like an orientation or a motion direction will increase the response of neurons preferring the attended feature (response gain) rather than increase the sensory input strength of the attended stimulus (input gain). This effect of feature-based attention on neuronal responses should translate to similar patterns of improvement in behavioral performance, with psychometric functions showing response gain rather than input gain when attention is directed to the task-relevant feature. In contrast, we report here that when human subjects are cued to attend to one of two motion directions in a transparent motion display, attentional effects manifest as a combination of input and response gain. Further, the impact on input gain is greater when attention is directed towards a narrow range of motion directions than when it is directed towards a broad range. These results are captured by an extended NMoA, which either includes a stimulus-independent attentional contribution to normalization or utilizes direction-tuned normalization. The proposed extensions are consistent with the feature-similarity gain model of attention and the attentional modulation in extrastriate area MT, where neuronal responses are enhanced and suppressed by attention to preferred and non-preferred motion directions respectively.

Spatial representation and cognitive modulation of response variability in the lateral intraparietal area priority map.

The lateral intraparietal area (LIP) in the macaque contains a priority-based representation of the visual scene. We previously showed that the mean spike rate of LIP neurons is strongly influenced by spatially wide-ranging surround suppression in a manner that effectively sharpens the priority map. Reducing response variability can also improve the precision of LIP's priority map. We show that when a monkey plans a visually guided delayed saccade with an intervening distractor, variability (measured by the Fano factor) decreases both for neurons representing the saccade goal and for neurons representing the broad spatial surround. The reduction in Fano factor is maximal for neurons representing the saccade goal and steadily decreases for neurons representing more distant locations. LIP Fano factor changes are behaviorally significant: increasing expected reward leads to lower variability for the LIP representation of both the target and distractor locations, and trials with shorter latency saccades are associated with lower Fano factors in neurons representing the surround. Thus, the LIP Fano factor reflects both stimulus and behavioral engagement. Quantitative modeling shows that the interaction between mean spike count and target-receptive field (RF) distance in the surround during the predistractor epoch is multiplicative: the Fano factor increases more steeply with mean spike count further away from the RF. A negative-binomial model for LIP spike counts captures these findings quantitatively, suggests underlying mechanisms based on trial-by-trial variations in mean spike rate or burst-firing patterns, and potentially provides a principled framework to account simultaneously for the previously observed unsystematic relationships between spike rate and variability in different brain areas.

Extrafoveal preview benefit during free-viewing visual search in the monkey.

Previous studies have shown that subjects require less time to process a stimulus at the fovea after a saccade if they have viewed the same stimulus in the periphery immediately prior to the saccade. This extrafoveal preview benefit indicates that information about the visual form of an extrafoveally viewed stimulus can be transferred across a saccade. Here, we extend these findings by demonstrating and characterizing a similar extrafoveal preview benefit in monkeys during a free-viewing visual search task. We trained two monkeys to report the orientation of a target among distractors by releasing one of two bars with their hand; monkeys were free to move their eyes during the task. Both monkeys took less time to indicate the orientation of the target after foveating it, when the target lay closer to the fovea during the previous fixation. An extrafoveal preview benefit emerged even if there was more than one intervening saccade between the preview and the target fixation, indicating that information about target identity could be transferred across more than one saccade and could be obtained even if the search target was not the goal of the next saccade. An extrafoveal preview benefit was also found for distractor stimuli. These results aid future physiological investigations of the extrafoveal preview benefit.

Surround suppression sharpens the priority map in the lateral intraparietal area.

In the visual world, stimuli compete with each other for allocation of the brain's limited processing resources. Computational models routinely invoke wide-ranging mutually suppressive interactions in spatial priority maps to implement active competition for attentional and saccadic allocation, but such suppressive interactions have not been physiologically described, and their existence is controversial. Much evidence implicates the lateral intraparietal area as a candidate priority map in the macaque (Macaca mulatta). Here, we demonstrate that the responses of neurons in the lateral intraparietal area (LIP) to a task-irrelevant distractor are strongly suppressed when the monkey plans saccades to locations outside their receptive fields. Suppression can be evoked both by flashed visual stimuli and by a memorized saccade plan. The suppressive surrounds of LIP neurons are spatially tuned and wide ranging. Increasing the monkey's motivation enhances target-distractor discriminability by enhancing both distractor suppression and the saccade goal representation; these changes are accompanied by correlated improvements in behavioral performance.

Saccade-synchronized rapid attention shifts in macaque visual cortical area MT.

While making saccadic eye-movements to scan a visual scene, humans and monkeys are able to keep track of relevant visual stimuli by maintaining spatial attention on them. This ability requires a shift of attentional modulation from the neuronal population representing the relevant stimulus pre-saccadically to the one representing it post-saccadically. For optimal performance, this trans-saccadic attention shift should be rapid and saccade-synchronized. Whether this is so is not known. We trained two rhesus monkeys to make saccades while maintaining covert attention at a fixed spatial location. We show that the trans-saccadic attention shift in cortical visual medial temporal (MT) area is well synchronized to saccades. Attentional modulation crosses over from the pre-saccadic to the post-saccadic neuronal representation by about 50 ms after a saccade. Taking response latency into account, the trans-saccadic attention shift is well timed to maintain spatial attention on relevant stimuli, so that they can be optimally tracked and processed across saccades.

Coupling between One-Dimensional Networks Reconciles Conflicting Dynamics in LIP and Reveals Its Recurrent Circuitry.

Little is known about the internal circuitry of the primate lateral intraparietal area (LIP). During two versions of a delayed-saccade task, we found radically different network dynamics beneath similar population average firing patterns. When neurons are not influenced by stimuli outside their receptive fields (RFs), dynamics of the high-dimensional LIP network during slowly varying activity lie predominantly in one multi-neuronal dimension, as described previously. However, when activity is suppressed by stimuli outside the RF, slow LIP dynamics markedly deviate from a single dimension. The conflicting results can be reconciled if two LIP local networks, each underlying an RF location and dominated by a single multi-neuronal activity pattern, are suppressively coupled to each other. These results demonstrate the low dimensionality of slow LIP local dynamics, and suggest that LIP local networks encoding the attentional and movement priority of competing visual locations actively suppress one another.

Visual attention is available at a task-relevant location rapidly after a saccade.

Maintaining attention at a task-relevant spatial location while making eye-movements necessitates a rapid, saccade-synchronized shift of attentional modulation from the neuronal population representing the task-relevant location before the saccade to the one representing it after the saccade. Currently, the precise time at which spatial attention becomes fully allocated to the task-relevant location after the saccade remains unclear. Using a fine-grained temporal analysis of human peri-saccadic detection performance in an attention task, we show that spatial attention is fully available at the task-relevant location within 30 milliseconds after the saccade. Subjects tracked the attentional target veridically throughout our task: i.e. they almost never responded to non-target stimuli. Spatial attention and saccadic processing therefore co-ordinate well to ensure that relevant locations are attentionally enhanced soon after the beginning of each eye fixation.

A rapid and precise on-response in posterior parietal cortex.

The activity of neurons in the lateral intraparietal area (LIP) of the monkey predicts the monkey's allocation of spatial attention. We show here that despite being relatively high within the visual hierarchy, neurons in LIP have extremely short and precise visual latencies. Mean latency was 45.2 msec; the timing precision of the onset response was usually better than 4 msec. The majority of neurons had a pause in response after an initial burst, followed by more sustained visual activity. Previous attention allocation had no effect on either the latency or magnitude of the initial burst, but produced clear effects on the magnitude of the later sustained activity. Together, these data indicate that the initial burst in LIP visual response reflects an uncontaminated sensory signal. Information about stimulus onset is transmitted rapidly through the visual system to LIP; the on-response has a higher speed and temporal precision than realized previously. This information could be used to orient attention to novel objects in the visual environment rapidly and reliably.

Comment on "Auditory-nerve first-spike latency and auditory absolute threshold: a computer model" [J. Acoust. Soc. Am. 119, 406-417 (2006)].

A recent paper by Meddis [J. Acoust. Soc. Am. 119, 406-417 (2006)] shows that an existing model of the auditory nerve [Meddis and O'Mard, J. Acoust. Soc. Am. 117, 3787-3798 (2005)] is consistent with experimentally-measured first-spike latencies in the auditory nerve [Heil and Neubauer, J. Neurosci. 21, 7404-7415 (2001)]. The paper states that this consistency emerges because in the model, the calcium concentration inside the inner hair cell builds up over long periods of time (up to at least 200 ms) during tone presentation. It further states that integration over long time-scales happens despite the very short time constants (< 1 ms) used for the calcium dynamics. This letter demonstrates that these statements are incorrect. It is shown by simulation that calcium concentration inside the hair cell stage of the Meddis model rapidly reaches a steady state within a few milliseconds of a stimulus onset, exactly as expected from the short time-constant in the simple first-order differential equation used to model the calcium concentration. The success of the Meddis model in fitting experimental data actually confirms earlier results [Krishna, J. Comput. Neurosci. 13, 71-91 (2002a)] that show that the experimental data are a natural result of stochasticity in the synaptic events leading up to spike-generation in the auditory nerve; integration over long time scales is not necessary to model the experimental data.

Reaction times of manual responses to a visual stimulus at the goal of a planned memory-guided saccade in the monkey.

Monkeys demonstrate improved contrast sensitivity at the goal of a planned memory-guided saccade (Science 299:81-86, 2003). Such perceptual improvements have been ascribed to an endogenous attentional advantage induced by the saccade plan. Speeded reaction times have also been used as evidence for attention. We therefore asked whether the attentional advantage at the goal of a planned memory-guided saccade led to speeded manual reaction times following probes presented at the saccade goal in a simple detection task. We found that monkeys showed slower manual reaction times when the probe appeared at the memorized goal of the planned saccade when compared to manual reaction times following a probe that appeared opposite the saccade goal. Flashing a distractor at the saccade goal after target presentation appeared to slow reaction times further. Our data, combined with prior results, suggest that a spatially localized inhibition operates on the neural representation of the saccade goal. This inhibition may be closely related or identical to the processes underlying inhibition-of-return. We also found that if the same detection task was interleaved with a difficult perceptual discrimination task, manual reaction times became faster when the probe was at the saccade goal. We interpret these results as being an effect of task difficulty; the more difficult interleaved task may have engaged endogenous attentional resources more effectively, allowing it to override the inhibition at the saccade goal. We construct and discuss a simple working hypothesis for the relationship between the effects of prior attention on neural activity in salience maps and on performance in detection and discrimination tasks.

A unified mechanism for spontaneous-rate and first-spike timing in the auditory nerve.

Recent physiological experiments have provided detailed descriptions of the properties of first-spike latency and variability in auditory cortex and nerve in response to pure tones with different envelopes. The envelope-dependence of first-spike timing and precision in auditory cortical neurons appears to reflect properties established in the nerve. First-spike latency properties in individual auditory nerve fibers are strongly correlated with their spontaneous rate (SR). It is shown here that a minimal, plausible model of auditory transduction with two free parameters accurately reproduces the physiological data from the auditory nerve population. The model consists of a simple gain stage, a bandpass filter, a rectifying saturating non-linearity, and a lowpass filter in series. The output of the lowpass filter drives an inhomogeneous Poisson process. The shape of the non-linearity is determined by SR; in physiological terms, this shape depends upon the resting sensitivity of the synapse between the inner hair cell and the auditory nerve. An alternative model for SR generation, where SR is added to the stimulus-driven output of a fixed nonlinearity, fails to account for the data. The results provide a novel, comprehensive and physiologically-based explanation for the range of experimental results on the envelope-dependence of first-spike latency and precision, and its relationship with SR, in the auditory system.