Activation of the Left Inferior Frontal Gyrus in the First 200 ms of Reading: Evidence from Magnetoencephalography (MEG)

Background

It is well established that the left inferior frontal gyrus plays a key role in the cerebral cortical network that supports reading and visual word recognition. Less clear is when in time this contribution begins. We used magnetoencephalography (MEG), which has both good spatial and excellent temporal resolution, to address this question.

Methodology/Principal Findings

MEG data were recorded during a passive viewing paradigm, chosen to emphasize the stimulus-driven component of the cortical response, in which right-handed participants were presented words, consonant strings, and unfamiliar faces to central vision. Time-frequency analyses showed a left-lateralized inferior frontal gyrus (pars opercularis) response to words between 100–250 ms in the beta frequency band that was significantly stronger than the response to consonant strings or faces. The left inferior frontal gyrus response to words peaked at ∼130 ms. This response was significantly later in time than the left middle occipital gyrus, which peaked at ∼115 ms, but not significantly different from the peak response in the left mid fusiform gyrus, which peaked at ∼140 ms, at a location coincident with the fMRI–defined visual word form area (VWFA). Significant responses were also detected to words in other parts of the reading network, including the anterior middle temporal gyrus, the left posterior middle temporal gyrus, the angular and supramarginal gyri, and the left superior temporal gyrus.

Conclusions/Significance

These findings suggest very early interactions between the vision and language domains during visual word recognition, with speech motor areas being activated at the same time as the orthographic word-form is being resolved within the fusiform gyrus. This challenges the conventional view of a temporally serial processing sequence for visual word recognition in which letter forms are initially decoded, interact with their phonological and semantic representations, and only then gain access to a speech code.     

Parallel visual motion processing streams for manipulable objects and human movements

We tested the hypothesis that different regions of lateral temporal cortex are specialized for processing different types of visual motion by studying the cortical responses to moving gratings and to humans and manipulable objects (tools and utensils) that were either stationary or moving with natural or artificially generated motions. Segregated responses to human and tool stimuli were observed in both ventral and lateral regions of posterior temporal cortex. Relative to ventral cortex, lateral temporal cortex showed a larger response for moving compared with static humans and tools. Superior temporal cortex preferred human motion, and middle temporal gyrus preferred tool motion. A greater response was observed in STS to articulated compared with unarticulated human motion. Specificity for different types of complex motion (in combination with visual form) may be an organizing principle in lateral temporal cortex.     

Methods for the identification of evoked response components in the frequency and combined time/frequency domains

Two prominent frequency components designated f1 and f2 have been identified in the visual evoked response to the transient presentation of sinusoidal luminance gratings in the range of 0.5–8 c/deg. The components occur at temporal frequencies below the alpha band, with the f1 frequency roughly half that of the f2 frequency. The f1 component is largest at low spatial frequencies with f2 becoming progressively dominant as spatial frequency is increased.The frequency and amplitude of f1 and f2 change substantially over the time course of the response. This has been studied by calculating the temporal frequency spectrum of the transient evoked potential over successive short-time epochs running through the response. Using this technique, the response is shown to consist of narrow- and frequency peaks or ‘formants’ emerging at different times after stimulus onset. These formants occur at frequencies other than those of the spontaneous EEG and undergo changes in frequency and amplitude over the time course of the response.Two spectrum analysis techniques were employed: the Discrete Fourier Transform and Linear Predictive Coding. Frequency components were successfully identified in single-trial responses using the LPC technique.     

Dark rearing alters the normal development of spatiotemporal response properties but not of contrast detection threshold in mouse retinal ganglion cells

The mouse visual system is immature when the eyes open two weeks after birth. As in other mammals, some of the maturation that occurs in the subsequent weeks is known to depend on visual experience. Development of the retina, which as the first stage of vision provides the visual information to the brain, also depends on light‐driven activity for proper development but has been less well studied than visual cortical development. The critical properties for retinal encoding of images include detection of contrast and responsiveness to the broad range of temporal stimulus frequencies present in natural stimuli. Here we show that contrast detection threshold and temporal frequency response characteristics of ON and OFF retinal ganglion cells (RGCs), which are poor at eye opening, subsequently undergo maturation, improving RGC performance. Further, we find that depriving mice of visual experience from before birth by rearing them in the dark causes ON and OFF RGCs to have smaller receptive field centers but does not affect their contrast detection threshold development. The modest developmental increase in temporal frequency responsiveness of RGCs in mice reared on a normal light cycle was inhibited by dark rearing only in ON but not OFF RGCs. Thus, these RGC response characteristics are in many ways unaffected by the experience‐dependent changes to synaptic and spontaneous activity known to occur in the mouse retina in the two weeks after eye opening, but specific differences are apparent in the ON vs. OFF RGC populations. © 2014 Wiley Periodicals, Inc. Develop Neurobiol 74: 692–706, 2014     

Characteristics of Human Luminance Discrimination and Modeling a Neural Network Based on the Response Properties of the Visual Cortex

Reaction time (RT) and error rate that depend on stimulus duration were measured in a luminance-discrimination reaction time task. Two patches of light with different luminance were presented to participants for ‘short’ (150 ms) or ‘long’ (1 s) period on each trial. When the stimulus duration was ‘short’, the participants responded more rapidly with poorer discrimination performance than they did in the longer duration. The results suggested that different sensory responses in the visual cortices were responsible for the dependence of response speed and accuracy on the stimulus duration during the luminance-discrimination reaction time task. It was shown that the simple winner-take-all-type neural network model receiving transient and sustained stimulus information from the primary visual cortex successfully reproduced RT distributions for correct responses and error rates. Moreover, temporal spike sequences obtained from the model network closely resembled to the neural activity in the monkey prefrontal or parietal area during other visual decision tasks such as motion discrimination and oddball detection tasks.     

Spectral Characteristics of Phase Sensitivity and Discharge Rate of Neurons in the Ascending Tectofugal Visual System

Drifting gratings can modulate the activity of visual neurons at the temporal frequency of the stimulus. In order to characterize the temporal frequency modulation in the cat’s ascending tectofugal visual system, we recorded the activity of single neurons in the superior colliculus, the suprageniculate nucleus, and the anterior ectosylvian cortex during visual stimulation with drifting sine-wave gratings. In response to such stimuli, neurons in each structure showed an increase in firing rate and/or oscillatory modulated firing at the temporal frequency of the stimulus (phase sensitivity). To obtain a more complete characterization of the neural responses in spatiotemporal frequency domain, we analyzed the mean firing rate and the strength of the oscillatory modulations measured by the standardized Fourier component of the response at the temporal frequency of the stimulus. We show that the spatiotemporal stimulus parameters that elicit maximal oscillations often differ from those that elicit a maximal discharge rate. Furthermore, the temporal modulation and discharge-rate spectral receptive fields often do not overlap, suggesting that the detection range for visual stimuli provided jointly by modulated and unmodulated response components is larger than the range provided by a one response component.     

Recognition of the spatially transformed objects in men and women: an analysis of the behavior and evoked potentials

In 16 men and 15 women analyzed the accuracy, reaction time and visual evoked potentials during the recognition of familiar objects at different levels of spatial transformation. We used the three levels of transformation: in a fixed position relative to each other details were carried out (1) the displacement of all the details in the radial direction and (2 and 3) a similar shift in conjunction with the rotation of all the details of the figure by +/- 0-45 and +/- 45-90 degrees. The task performance was not dependent on gender: the transformation of the image led to a deterioration of identification with the most identification impairment in the case of maximal details' rotation. Changes in evoked potentials (ERP) are different for men and women. Only in men early (100 ms after stimulus) response of the parietal cortex associated with the level of figure transformation: the more rotation evoked the higher the response. In women figure transformation evoked the ERP changes in the time window of negativity N170, they are associated with figure ungrouping but not with details rotation, and are localized in other visual areas--occipital and temporal. The data obtained are discussed in light of theory of gender specificity of the visual representations of space.     

Rapid dynamics of contrast responses in the cat primary visual cortex

The visual information we receive during natural vision changes rapidly and continuously. The visual system must adapt to the spatiotemporal contents of the environment in order to efficiently process the dynamic signals. However, neuronal responses to luminance contrast are usually measured using drifting or stationary gratings presented for a prolonged duration. Since motion in our visual field is continuous, the signals received by the visual system contain an abundance of transient components in the contrast domain. Here using a modified reverse correlation method, we studied the properties of responses of neurons in the cat primary visual cortex to different contrasts of grating stimuli presented statically and transiently for 40 ms, and showed that neurons can effectively discriminate the rapidly changing contrasts. The change in the contrast response function (CRF) over time mainly consisted of an increment in contrast gain (CRF shifts to left) in the developing phase of temporal responses and a decrement in response gain (CRF shifts downward) in the decay phase. When the distribution range of stimulus contrasts was increased, neurons demonstrated decrement in contrast gain and response gain. Our results suggest that contrast gain control (contrast adaptation) and response gain control mechanisms are well established during the first tens of milliseconds after stimulus onset and may cooperatively mediate the rapid dynamic responses of visual cortical neurons to the continuously changing contrast. This fast contrast adaptation may play a role in detecting contrast contours in the context of visual scenes that are varying rapidly.     

Effects of Near-Threshold Stimulation of the Vestibular Apparatus on Postural Responses Evoked by Displacements of the Visualized Surrounding

In healthy subjects in the relaxed upward stance and perceiving a virtual visual environment (VVE), we recorded postural reactions to isolated visual and vestibular stimulations or their combinations. Lateral displacements of the visualized virtual scene were used as visual stimuli. The vestibular apparatus was stimulated by application of near-threshold galvanic current pulses to the proc. mastoidei of the temporal bones. Isolated VVE shifts evoked mild, nonetheless clear, body tilts readily distinguished in separate trials; at the same time, postural effects of isolated vestibular stimulation could be detected only after averaging of several trials synchronized with respect to the beginning of stimulation. Under conditions of simultaneous combined presentation of visual and vestibular stimuli, the direction of the resulting postural responses always corresponded to the direction of responses induced by VVE shifts. The contribution of an afferent volley from the vestibular organ depended on the coincidence/mismatch of the direction of motor response evoked by such a volley with the direction of response to visual stimulation. When both types of stimulations evoked unidirectional body tilts, postural responses were facilitated, and the resulting effect was greater than that of simple summation of the reactions to isolated actions of the above stimuli. In the case where isolated galvanic stimulation evoked a response opposite with respect to that induced by visual stimulation, the combined action of these stimuli of different modalities evoked postural responses identical in their magnitude, direction, and shape to those evoked by isolated visual stimulation. The above findings allow us to conclude that the effects of visual afferent input on the vertical posture under conditions of our experiments clearly dominate. In general, these results confirm the statement that neuronal structures involved in integrative processing of different afferent volleys preferably select certain type of afferentation carrying more significant or more detailed information on displacements (including oscillations) of the body in space.     

Dynamics of light intensity detection by visual cortical neurons in cats

The dynamics of the intensity function of 32 neurons in area 17 of the visual cortex to photic stimuli of optimal size, shape, and orientation flashing in the center of the receptive field was studied by the time slices method, with a step of 10 or 20 msec, in unanesthetized, curarized cats. All neurons tested showed instability of their intensity function reflected in characteristics of successive fragments of the response: It changed both in preferred intensity and in width of the intensity range within which the neuron generated an above-threshold response. In 72% of cases the preferred intensity for the neuron changed successively during the 4–200 msec after the beginning of stimulation by 4–36 dB from greater toward lesser brightnesses, but later it changed more rapidly (in 20–60 msec), rising again apparently in a jump. In four cases the response optimum was shifted up the intensity scale from its initial value by 10–20 dB. Analysis showed that the observed effects are the simple result of the shape of the relationship between temporal characteristics of the response (latent period, time taken to reach the maximum, and time of ending of the burst) to photic stimulus intensity. The possible functional role of these effects for dynamic time coding of information on brightness of photic stimuli by visual cortical neurons is discussed.     

Temporal fidelity in the visual system.

The temporal properties of the visual system have been analyzed by recording the ERG and its isolated components in response to light stimuli whose luminance was varied sinusoidally. The performance of the visual system to periodic light stimuli was tested in human subjects psychophysically. The comparison of the results in control conditions and after administration of drugs that specifically block the hyperpolarization activated current (Ih) suggest that the inner rectifying properties of the inner segment membrane of rods is involved in a process of temporal differentiation of the visual signals whereby high frequency components of the response especially relevant for the visual performance are enhanced. It is proposed that the temporal fidelity of the visual system is the results of an elaboration starting at early level of the signal generated by the phototransductive cascade.     

Integration of auditory and visual information about objects in superior temporal sulcus

Two categories of objects in the environment-animals and man-made manipulable objects (tools)-are easily recognized by either their auditory or visual features. Although these features differ across modalities, the brain integrates them into a coherent percept. In three separate fMRI experiments, posterior superior temporal sulcus and middle temporal gyrus (pSTS/MTG) fulfilled objective criteria for an integration site. pSTS/MTG showed signal increases in response to either auditory or visual stimuli and responded more to auditory or visual objects than to meaningless (but complex) control stimuli. pSTS/MTG showed an enhanced response when auditory and visual object features were presented together, relative to presentation in a single modality. Finally, pSTS/MTG responded more to object identification than to other components of the behavioral task. We suggest that pSTS/MTG is specialized for integrating different types of information both within modalities (e.g., visual form, visual motion) and across modalities (auditory and visual).     

A Nonlinear Model of the Behavior of Simple Cells in Visual Cortex

Despite their structured receptive fields (RFs) and the strong linear components in their responses, most simple cells in mammalian visual cortex exhibit nonlinear behaviors. Besides the contrast-response function, nonlinearities are evident in various types of failure at superposition tasks, in the disagreement between direction indices computed from drifting and counterphase flickering gratings, in various forms of response suppression (including end- and side-stopping, spatial-frequency-specific inhibition and cross-orientation inhibition), in the advance of phase with increasing contrast, and in phase-insensitive and frequency-doubled responses to counterphase flickering gratings. These behaviors suggest that nonlinearities are involved in the operation of simple cells, but current models fail to explain them. A quantitative model is presented here that purports to describe basic and common principles of operation for all visual cortical cells. Simple cells are described as receiving afferents from multiple subunits that differ in their individual RFs and temporal impulse responses (TIRs). Subunits are independent and perform a spatial integration across their RFs followed by halfwave rectification and temporal convolution with their TIRs. This parallel operation yields a set of temporal functions representing each subunit's contribution to the membrane potential of the host cell, whose final form is given by the weighted sum of all subunits' contributions. By varying the number of subunits and their particular characteristics, different instances of the model are obtained each of which displays a different set of behaviors. Extensive simulation results are presented that illustrate how all of the reported nonlinear behaviors of simple cells arise from these multi-subunit organizations.     

Adaptation of transient responses of a movement-sensitive neuron in the visual system of the blowfly Calliphora erythrocephala

We studied temporal response properties of the H1 neuron by extracellular recording. This neuron is a wide-field movement-sensitive element in the visual system of the blowfly (Calliphora erythrocephala). If the neuron is stimulated with a stepwise pattern displacement in its preferred direction, it responds with a burst of action potentials. By repeating the stimulus step one obtains the average of the step response: a 20ms latency time followed by a sharp increase in average firing rate and a slower decay to the resting activity. We report that the characteristic decay time of the step response depends on the stimulus history. If the stimulus moved prior to the step, the higher the pattern velocity, the faster was the decay of the step response to the resting level. In quantitative terms, for velocities in the range 0.4–100°/s, the decay time-constant varies from 300–10ms and is smaller for higher velocities. The time-constant is only weakly affected by other stimulus parameters such as modulation depth or spatial wavelength, and is set independently in different areas of the visual field where it is tuned to the local velocity. We discuss a possible advantage of this form of adaptation for the processing of visual signals: The performance of the nolinear operations that extract information from the visual input can be optimized by prefiltering signals in the individual visual columns with a time-constant that decreases with stimulus velocity. It will be shown that both the test step response and the response to continuous movement can be described reasonably well by a correlation model with input filters that adapt their time-constants.     

Dynamic Electrode-to-Image (DETI) mapping reveals the human brain’s spatiotemporal code of visual information

A number of neuroimaging techniques have been employed to understand how visual information is transformed along the visual pathway. Although each technique has spatial and temporal limitations, they can each provide important insights into the visual code. While the BOLD signal of fMRI can be quite informative, the visual code is not static and this can be obscured by fMRI’s poor temporal resolution. In this study, we leveraged the high temporal resolution of EEG to develop an encoding technique based on the distribution of responses generated by a population of real-world scenes. This approach maps neural signals to each pixel within a given image and reveals location-specific transformations of the visual code, providing a spatiotemporal signature for the image at each electrode. Our analyses of the mapping results revealed that scenes undergo a series of nonuniform transformations that prioritize different spatial frequencies at different regions of scenes over time. This mapping technique offers a potential avenue for future studies to explore how dynamic feedforward and recurrent processes inform and refine high-level representations of our visual world.     

Spatiotemporal organization of simple-cell receptive fields in area 18 of cat’s cortex

Spatiotemporal structures of receptive-fields (RF) have been studied for simple cells in area 18 of eat by measuring the temporal transfer function (TTF) over different locations (subregions) within the RF. The temporal characteristics of different subregions differed from each other in the absolute phase shift (APS) to visual stimuli. Two types of relationships can be seen: (i)The APS varied continuously from one subregion to the next: (ii) A 180°-phase jump was seen as the stimulus position changed somewhere within the receptive field. Spatiotemporal receptive field profiles have been determined by applying reverse Fourier analysis to responses in the frequency domain. For the continuous type, spatial and temporal characteristics cannot be dissociated (space time inseparable) and the spatiotemporal structure is oriented. On the contrary, the spatial and temporal characteristics for the jumping type can be dissociated (space-time separable) and the structure is not oriented in the space-time plane. Based on the APSs measured at different subregions, the optimal direction of motion and optimal spatial frequency of neurons can be predicted.     

Differences in functional organization of the visual center in frogs and cats

Functional characteristics of responses of tectal neurons in the frog and the primary visual cortex of the cat obtained under indentical experimental conditions during changes in the brightness and duration of flashes within the range of 6 log units were compared. In frogs most units have short summation times and relatively lower thresholds; the response latency is 5–7 times longer than in cats. The overwhelming majority of tectal units can respond only to a narrow range of photic energy that differs for different cells. Most cells in cats respond to changes in brightness of between 4 and 5 log units; they have long summation times, short latent periods, and relatively higher thresholds. The differences found on comparison of the various functional characteristics of the cells in the visual center show that frogs have fixed mechanisms of temporal and spatial interaction responsibile for detection of stimulus brightness. In cats this interaction between individual cell populations and this mutual inhibition between adjacent cells are not prominent. The increased complexity and overlapping of interneuronal connections leads to convergence of day and twilight vision stimuli on the same neuron and to the ability of single units to respond to the whole "working" range of light brightness for the cat visual system.     

Spatiotemporal organization of simple-cell receptive fields in area 18 of cat''s cortex

Spatiotemporal structures of receptive-fields (RF) have been studied for simple cells in area 18 of eat by measuring the temporal transfer function (TTF) over different locations (subregions) within the RF. The temporal characteristics of different subregions differed from each other in the absolute phase shift (APS) to visual stimuli. Two types of relationships can be seen: (i)The APS varied continuously from one subregion to the next: (ii) A 180°-phase jump was seen as the stimulus position changed somewhere within the receptive field. Spatiotemporal receptive field profiles have been determined by applying reverse Fourier analysis to responses in the frequency domain. For the continuous type, spatial and temporal characteristics cannot be dissociated (space time inseparable) and the spatiotemporal structure is oriented. On the contrary, the spatial and temporal characteristics for the jumping type can be dissociated (space-time separable) and the structure is not oriented in the space-time plane. Based on the APSs measured at different subregions, the optimal direction of motion and optimal spatial frequency of neurons can be predicted. Project supported by the National Natural Science Foundation of China (Grant Nos. 39570206, 39330110) and the Laboratory of Visual Information Processing, Chinese Academy of Sciences.     

Modeling the Dynamics of Sensory Reweighting

Reweighting sensory information adaptively is considered critical for flexible postural control, but little is known of the time scale of the reweighting process. We analyzed the transient dynamics of sensory reweighting in a previously published nonlinear adaptive model of sensory integration in the human postural control system. The model’s dynamics of adaptation were tested in response to abrupt changes in the amplitude of the motion of the visual surround. In addition to qualitatively reproducing the correct asymptotic response to such changes in visual amplitude, as previously found, the model qualitatively reproduced the asymmetric transient response elucidated in recent experiments (Oie et al. in Gait Posture 2005). In particular, the model adapts at an initially rapid rate to a switch from low to high amplitude visual motion, but at an initially slower rate upon the return to low amplitude motion. The observed temporal asymmetry has potential functional value. Rapid downweighting of a visual stimulus that suddenly increases is necessary to prevent loss of upright equilibrium. A visual stimulus that decreases in amplitude does not pose a threat to upright balance, allowing for slower upweighting without functional consequence.     

See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex

Our understanding of multisensory integration has advanced because of recent functional neuroimaging studies of three areas in human lateral occipito-temporal cortex: superior temporal sulcus, area LO and area MT (V5). Superior temporal sulcus is activated strongly in response to meaningful auditory and visual stimuli, but responses to tactile stimuli have not been well studied. Area LO shows strong activation in response to both visual and tactile shape information, but not to auditory representations of objects. Area MT, an important region for processing visual motion, also shows weak activation in response to tactile motion, and a signal that drops below resting baseline in response to auditory motion. Within superior temporal sulcus, a patchy organization of regions is activated in response to auditory, visual and multisensory stimuli. This organization appears similar to that observed in polysensory areas in macaque superior temporal sulcus, suggesting that it is an anatomical substrate for multisensory integration. A patchy organization might also be a neural mechanism for integrating disparate representations within individual sensory modalities, such as representations of visual form and visual motion.