Saccades and the flow of visual information in the occipitotemporal
pathway.
Long-range corticocortical connections form the conduits of information
exchange between the specialized functional domains found throughout the cerebral
cortex. The successful performance of many perceptual and behavioral tasks may rely on
establishing and maintaining specific patterns of neural activity in these long-range
connections. The dynamics of corticocortical communication may be influenced, in part,
by the motor actions produced during a behavior. In the visual system, saccadic eye
movements influence the activity of individual neurons (as seen in single-unit and
multiunit recordings) and large populations of neurons (as seen in scalp potentials and
local field potentials). Since saccades produce alterations in visual perception and task
performance it is possible that large-scale integration may be influenced and perhaps
organized around such motor behavior. We examined how saccades influence the activity
of local populations of neurons and their interactions in the occipitotemporal pathway of
alert monkeys.
Monkeys were rewarded for recognizing a particular configuration of a set of
geometric features from a periodically modulated temporal sequence of visual patterns.
The monkeys were allowed to make saccadic eye movements during the trials when the
goal of the trial was pattern recognition. The two monkeys utilized individualized but
stereotyped scan paths during the pattern recognition trials. These scan paths developed
over the course of training and remained consistent over a period of two years. The same
visual display was also presented with the addition of a fixation cue. The monkeys were
rewarded on these trials for maintaining fixation at the position of the cursor.
Local field potentials (LFPs) and single and multi-unit activity were
simultaneously recorded with high-impedance (1-4 MOhm) microelectrodes from dual
sites within the visual cortex of alert monkeys. Recordings included occipital lobe (striate
and early extrastriate visual cortices) and temporal lobe (TE and STS) pairs and pairs
from the occipital lobes of both hemispheres. The analysis of the neural data exploited
two different types of averaging triggers: (1) an external trigger provided by the periodic
modulation of the visual stimulus; (2) an internal trigger derived from saccade initiation
times. The analysis time windows for samples referenced to the visual stimulus were set
by the periods of periodic stimulation; i.e. 250 ms, 330 ms and 500 ms for the 4 Hz, 3 Hz,
and 2 Hz modulated stimuli. The averages constructed with the saccade triggers were
500 ms in the length centered on the saccade initiation time.
Single-unit recordings demonstrated periods of suppressed firing prior to and
during saccades in many cortical areas. Periods of enhanced firing were seen following
saccades in both occipital and temporal lobe sites. Periods of enhanced firing prior to
saccades were also seen in occipital lobe sites. The latency of interaction between
occipital and temporal lobe sites was ~80 msec during fixation. Saccades broadened the
distribution of latencies.
LFPs were analyzed by calculating time-frequency spectrograms and the timefrequency coherence of the LFPs recorded at paired sites from prewhitened residual
signals extracted from individual trials. We computed the spectrograms and timefrequency coherence using an algorithm developed by D. Thomson and P. Mitra of Bell
Labs/Lucent Technologies. The multi-taper spectrogram is computed for each trial by
convolving each spectral estimate with a series of cross-products formed between all of
the tapers used in calculating the spectrum. The ‘Slepian’ functions (discrete prolate
spheriodal sequences) were used as the tapers. The spectrograms have a resolution limit
in the frequency and time domain established by the time-frequency bandwidth. This
bandwidth is controlled by the number of Slepian tapers used to produce independent
estimates of the spectrum. The frequency resolution is 2*W, where W is the halffrequency bandwidth of the spectrum. The time resolution is given by 2*W*T where T is
the duration of each sample in the ensemble.
The LFPs were also analyzed by calculating time-frequency spectrograms from
the average waveforms using a series of temporally overlapping Slepian tapers. The
spectrograms simplify the characterization of the saccade-driven activity in the LFP in
terms of time-frequency power. For example, it is often difficult to determine the latency
to peak activation of an LFP or VEP when working directly with the multi-phasic voltage
trajectories in the time-domain. The spectrograms present regions in time-frequency
space that are only positive in power.
The average LFPs produced by local populations in the occipital lobe exhibited
well-defined concentrations in power in time-frequency following the onset of a saccade
(~60-80 msec). For the temporal lobe sites, the episodes of significant activation were
constrained to lower frequencies, less localized in time, less influenced by saccade
metrics than in the occipital lobe, and often initiated prior to saccades. Analysis of the
variance spectra (true power spectral estimates) revealed more temporally sustained
broadband local population activity in the occipital lobe prior to the generation of
leftward saccades. More power was seen in the LFPs in the postsaccadic epoch when the
saccade was directed to the right. Corticocortical synchronization was often dominated by
activity in the beta frequency band (15-30 Hz). The presence of saccades produced
transient increases in coherence between some cortical sites while disrupting bouts of
coherence at other cortical sites. In general, there was more evidence for common source
inputs to the coherence in the pair recordings drawn from the two occipital lobes.
The goal of this study was to describe how the intrinsic dynamics in the neural
activity in the visual cortex could be influenced by the free-viewing behavior of the
monkey. In particular, we wanted to determine the extent to which the synchronization
between disparate cortical domains was influenced by the presence of saccades. Our
evidence suggests that it is possible for saccades to disrupt epochs of synchronization
among cortical regions throughout the visual pathway, and that saccades may be able to
provide a phase mark to initiate a new fast feedforward sweep through the cortical
hierarchy at the start of a fixation period. Changes in synchronization appear to be
frequency specific and may be as brief as 100 ms.