Alterations in functional thalamocortical connectivity following neonatal whisker trimming with adult regrowth.

Neonatal whisker trimming followed by adult whisker regrowth leads to higher responsiveness and altered receptive field properties of cortical neurons in corresponding layer 4 barrels. Studies of functional thalamocortical (TC) connectivity in normally reared adult rats have provided insights into how experience-dependent TC synaptic plasticity could impact the establishment of feedforward excitatory and inhibitory receptive fields. The present study employed cross-correlation analyses to investigate lasting effects of neonatal whisker trimming on functional connections between simultaneously recorded thalamic neurons and regular-spike (RS), presumed excitatory, and fast-spike (FS), presumed inhibitory, barrel neurons. We find that, as reported previously, RS and FS cells in whisker-trimmed animals fire more during the earliest phase of their whisker-evoked responses, corresponding to the arrival of TC inputs, despite a lack of change or even a slight decrease in the firing of thalamic cells that contact them. Functional connections from thalamus to cortex are stronger. The probability of finding TC-RS connections was twofold greater in trimmed animals and similar to the frequency of TC-FS connections in control and trimmed animals, the latter being unaffected by whisker trimming. Unlike control cases, trimmed RS units are more likely to receive inputs from TC units (TCUs) and have mismatched angular tuning and even weakly responsive TCUs make strong functional connections on them. Results indicate that developmentally appropriate tactile experience early in life promotes the differential thalamic engagement of excitatory and inhibitory cortical neurons that underlies normal barrel function.

Weaker feedforward inhibition accounts for less pronounced thalamocortical response transformation in mouse vs. rat barrels.

Feedforward inhibition is a common motif of thalamocortical circuits. Strong engagement of inhibitory neurons by thalamic inputs enhances response differentials between preferred and nonpreferred stimuli. In rat whisker-barrel cortex, robustly driven inhibitory barrel neurons establish a brief epoch during which synchronous or near-synchronous thalamic firing produces larger responses to preferred stimuli, such as high-velocity deflections of the principal whisker in a preferred direction. Present experiments in mice show that barrel neuron responses to preferred vs. nonpreferred stimuli differ less than in rats. In addition, fast-spike units, thought to be inhibitory barrel neurons, fire less robustly to whisker stimuli in mice than in rats. Analyses of real and simulated data indicate that mouse barrel circuitry integrates thalamic inputs over a broad temporal window, and that, as a consequence, responses of barrel neurons are largely similar to those of thalamic neurons. Results are consistent with weaker feedforward inhibition in mouse barrels. Differences in thalamocortical circuitry between mice and rats may reflect mechanical properties of the whiskers themselves.

Examining cognitive interference and adaptive safety behaviours in tactical vehicle control.

Concurrent mental workload degrades some aspects of driving performance, but drivers might be able to modify their behaviour adaptively to accommodate cognitive impairments. For example, they might maintain longer vehicle headway in dual-task conditions to compensate for slowed response times. Studies documenting such adaptive behaviours typically use steady-state driving scenarios such as car following. Yet, driving often involves tactical control situations in which drivers need to monitor multiple aspects of their traffic environment and to accommodate changing goals. In two simulator experiments, this study examined the impact of mental workload on safety margins (distances) that drivers keep when engaged in a tactical control task: passing other vehicles. Although drivers did increase their headway adaptively when engaged in steady-state car following (experiment 2), they did not adapt their behaviour to accommodate cognitive load when performing tactical control manoeuvres. Implications of this difference between steady-state and tactical control driving contexts, both for driving research and for driving safety, are discussed.

Adaptation in thalamic barreloid and cortical barrel neurons to periodic whisker deflections varying in frequency and velocity.

Layer IV circuitry in the rodent whisker-to-barrel pathway transforms the thalamic input signal spatially and temporally. Excitatory and inhibitory barrel neurons display response properties that differ from each other and from their common thalamic inputs. Here we further examine thalamocortical response transformations by characterizing the responses of individual thalamic barreloid neurons and presumed excitatory and inhibitory cortical barrel neurons to periodic whisker deflections varying in frequency from 1 to 40 Hz. Both pulsatile and sinusoidal periodic stimulation of fixed deflection amplitude were used to assess stimulus-evoked adaptation of thalamocortical units (TCUs), fast-spike barrel units (FSUs: presumed inhibitory neurons), and regular-spike barrel units (RSUs: presumed excitatory neurons). Monotonic, frequency-dependent reductions in firing were observed in thalamic and cortical neurons to the second and subsequent stimuli in trains of high (pulsatile)- and low (sinusoidal)-velocity deflections. RSUs and FSUs adapted substantially more than their thalamic input neurons, and at all frequencies, FSUs fired at higher rates than the other two cell types. For example at 40 Hz, response magnitudes of TCUs decreased by 34%, FSUs by 72%, and RSUs by 78%. Across frequencies, RSUs and FSUs displayed more cycle-by-cycle entrainment and phase-locked responses for (high velocity) pulsatile than (lower velocity) sinusoidal deflections; for TCUs, phase-locking was equivalent for both stimuli, but entrainment was higher for sinusoidal deflections. Strong feed-forward inhibition, in conjunction with synaptic depression, renders the firing of barrel neurons sparse but temporally faithful to the occurrence of repetitive whisker deflections, especially when they are of high velocity.

Axonal conduction properties of antidromically identified neurons in rat barrel cortex.

Physiological studies of the rodent somatosensory cortex have consistently described considerable heterogeneity in receptive field properties of neurons outside of layer IV, particularly those in layers V and VI. One such approach for distinguishing among different local circuits in these layers may be to identify the projection target of neurons whose axon collaterals contribute to the local network. In vivo, this can be accomplished using antidromic stimulation methods. Using this approach, the axonal conduction properties of cortical efferent neurons are described. Four projection sites were activated using electrical stimulation: (1) vibrissal motor cortex, (2) ventrobasal thalamus (VB), (3) posteromedial thalamic nucleus (POm), and (4) cerebral peduncle. Extracellular recordings were obtained from a total of 169 units in 21 animals. Results demonstrate a close correspondence between the laminar location of the antidromically identified neurons and their anatomically known layer of origin. Axonal properties were most distinct for corticofugal axons projecting through the crus cerebri. Corticothalamic axons projecting to either VB or POm were more similar to each other in terms of laminar location and conduction properties, but could be distinguished using focal electrical stimulation. It is concluded that, once stimulation parameters are adjusted for the small volume of the rat brain, the use of antidromic techniques may be an effective strategy to differentiate among projection neurons comprising different local circuits in supra- and infragranular circuits.

Processing in layer 4 of the neocortical circuit: new insights from visual and somatosensory cortex.

Recent experimental and theoretical results in cat primary visual cortex and in the whisker-barrel fields of rodent primary somatosensory cortex suggest common organizing principles for layer 4, the primary recipient of sensory input from the thalamus. Response tuning of layer 4 cells is largely determined by a local interplay of feed-forward excitation (directly from the thalamus) and inhibition (from layer 4 inhibitory interneurons driven by the thalamus). Feed-forward inhibition dominates excitation, inherits its tuning from the thalamic input, and sharpens the tuning of excitatory cells. Recurrent excitation enhances responses to effective stimuli.

How not to be seen: the contribution of similarity and selective ignoring to sustained inattentional blindness.

When people attend to objects or events in a visual display, they often fail to notice an additional, unexpected, but fully visible object or event in the same display. This phenomenon is now known as inattentional blindness. We present a new approach to the study of sustained inattentional blindness for dynamic events in order to explore the roles of similarity, distinctiveness, and attentional set in the detection of unexpected objects. In Experiment 1, we found that the similarity of an unexpected object to other objects in the display influences attentional capture: The more similar an unexpected object is to the attended items, and the greater its differencefrom the ignored items, the more likely it is that people will notice it. Experiment 2 explored whether this effect of similarity is driven by selective ignoring of irrelevant items or by selective focusing on attended items. The results of Experiment 3 suggest that the distinctiveness of the unexpected object alone cannot entirely account for the similarity effects found in the first two experiments; when attending to black items or white items in a dynamic display, nearly 30% of observers failed to notice a bright red cross move across the display, even though it had a unique color, luminance, shape, and motion trajectory and was visible for 5s. Together, the results suggest that inattentional blindness for ongoing dynamic events depends both on the similarity of the unexpected object to the other objects in the display and on the observer's attentional set.

Inhibition suppresses transmission of tonic vibrissa-evoked activity in the rat ventrobasal thalamus.

Previous studies have demonstrated that tonic responses of trigeminal ganglion neurons to maintained whisker deflections are transformed to mainly phasic responses in thalamocortical neurons. The high tonic responsiveness of thalamic reticular neurons suggests that thalamic inhibition may contribute to this suppression of tonic activity. To test this hypothesis we recorded responses of thalamocortical neurons in the ventroposterior medial (VPm) nucleus to 200 and 400 msec sustained whisker deflections during simultaneous microiontophoresis of the GABA receptor antagonists bicuculline and phaclofen. Under control conditions, VPm units responded to deflection plateaus with mean activities of only 18 spikes/sec, compared with 16 spikes/sec spontaneous firing. A minority of cells (5/19) had significantly greater plateau than spontaneous activity, and these cells were classified as tonic; the other 14/19 were considered phasic. Under GABA receptor antagonism, however, mean plateau activity increased to 53 spikes/sec compared with 30 spikes/sec spontaneous activity, and 7 of the 14 phasic units became tonically responsive. Increases in plateau activity were significantly greater, by both absolute and relative measures, than increases in spontaneous activity. Transient responses to stimulus onsets and offsets also increased in magnitude 4.0- and 2. 9-fold, attributable mainly to their increased duration. These data indicate that VPm neurons receive tonic excitatory inputs that under normal conditions are masked by inhibition. Suppression of tonic activity in VPm by inhibitory thalamic reticular neurons may reduce tonic inhibition in cortical layer IV circuits, preserving their responsiveness to transient signals.

Coding of deflection velocity and amplitude by whisker primary afferent neurons: implications for higher level processing.

Within the rat whisker-to-barrel pathway, local circuits in cortical layer IV are more sensitive to the initial timing of deflection-evoked thalamic responses than to the total number of spikes comprising them. Because thalamic response timing better reflects whisker deflection velocity than amplitude, cortical neurons are more responsive to the former than the latter. The aim of this study is to determine how deflection velocity and amplitude may be encoded by the primary afferent neurons innervating the vibrissae. Responses of 81 extracellularly recorded trigeminal ganglion neurons (60 slowly and 21 rapidly adapting) were studied using controlled whisker stimuli identical to those used previously to investigate the velocity and amplitude sensitivities of thalamic and cortical neurons. For either slowly (SA) or rapidly adapting (RA) neurons, velocity is reflected by both response magnitude, measured as the total number of evoked spikes/stimulus, and initial firing rate, measured as the number of spikes discharged during the first 2 ms of the response. Deflection amplitude, on the other hand, is represented only by the SA population in their response magnitudes. Thus, in both populations initial firing rates unambiguously reflect deflection velocity. Together with previous findings, results demonstrate that information about deflection velocity is preserved throughout the whisker-to-barrel pathway by central circuits sensitive to initial response timing.

High responsiveness and direction sensitivity of neurons in the rat thalamic reticular nucleus to vibrissa deflections.

The thalamic reticular nucleus (Rt) is strategically positioned to integrate descending and ascending signals in the control of sensorimotor and other thalamocortical activity. Its prominent role in the generation of sleep spindles notwithstanding, relatively little is known of Rt function in regulating interactions with the sensory environment. We recorded and compared the responses of individual Rt and thalamocortical neurons in the ventroposterior medial (VPm) nucleus of the rat to controlled deflections of mystacial vibrissae. Transient Rt responses to the onset (ON) and offset (OFF) of vibrissa deflection are larger and longer in duration than those of VPm and of all other populations studied in the whisker/barrel pathway. Magnitudes of ON and OFF responses in Rt were negatively correlated with immediately preceding activities, suggesting a contribution of low-threshold T-type Ca(2+) channels. Rt neurons also respond with high tonic firing rates during sustained vibrissa deflections. By comparison, VPm neurons are less likely to respond tonically and are more likely to exhibit tonic suppression. Rt and VPm populations are similar to each other, however, in that they retain properties of directional sensitivity established in primary afferent neurons. In both populations neurons are selective for deflection angle and exhibit directional consistency, responding best to a particular direction of movement regardless of the starting position of the vibrissal hair. These findings suggest a role for Rt in the processing of detailed sensory information. Temporally, Rt may function to limit the duration of stimulus-evoked VPm responses and to focus them on rapid vibrissa perturbations. Moreover, by regulating the baseline activity of VPm neurons, Rt may indirectly enhance the response selectivity of layer IV barrel neurons to synchronous VPm firing.

Circuit dynamics and coding strategies in rodent somatosensory cortex.

Previous experimental studies of both cortical barrel and thalamic barreloid neuron responses in rodent somatosensory cortex have indicated an active role for barrel circuitry in processing thalamic signals. Previous modeling studies of the same system have suggested that a major function of the barrel circuit is to render the response magnitude of barrel neurons particularly sensitive to the temporal distribution of thalamic input. Specifically, thalamic inputs that are initially synchronous strongly engage recurrent excitatory connections in the barrel and generate a response that briefly withstands the strong damping effects of inhibitory circuitry. To test this experimentally, we recorded responses from 40 cortical barrel neurons and 63 thalamic barreloid neurons evoked by whisker deflections varying in velocity and amplitude. This stimulus evoked thalamic response profiles that varied in terms of both their magnitude and timing. The magnitude of the thalamic population response, measured as the average number of evoked spikes per stimulus, increased with both deflection velocity and amplitude. On the other hand, the degree of initial synchrony, measured from population peristimulus time histograms, was highly correlated with the velocity of whisker deflection, deflection amplitude having little or no effect on thalamic synchrony. Consistent with the predictions of the model, the cortical population response was determined largely by whisker velocity and was highly correlated with the degree of initial synchrony among thalamic neurons (R(2) = 0.91), as compared with the average number of evoked thalamic spikes (R(2) = 0.38). Individually, the response of nearly all cortical cells displayed a positive correlation with deflection velocity; this homogeneity is consistent with the dependence of the cortical response on local circuit interactions as proposed by the model. By contrast, the response of individual thalamic neurons varied widely. These findings validate the predictions of the modeling studies and, more importantly, demonstrate that the mechanism by which the cortex processes an afferent signal is inextricably linked with, and in fact determines, the saliency of neural codes embedded in the thalamic response.

Change blindness in the absence of a visual disruption.

Findings from studies of visual memory and change detection have revealed a surprising inability to detect large changes to scenes from one view to the next ('change blindness'). When some form of disruption is introduced between an original and modified display, observers often fail to notice the change. This disruption can take many forms (e.g. an eye movement, a flashed blank screen, a blink, a cut in a motion picture, etc) with similar results. In all cases, the changes are sufficiently large that, were they to occur instantaneously, they would consistently be detected. Prior research on change blindness was predicated on the assumption that, in the absence of a visual disruption, the signal caused by the change would draw attention, leading to detection. In two experiments, we demonstrate that change blindness can occur even in the absence of a visual disruption. In one experiment, subjects actually detected more changes with a disruption than without one. When changes are sufficiently gradual, the visible change signal does not seem to draw attention, and large changes can go undetected. The findings are discussed in the context of metacognitive beliefs about change detection and the strategic decisions those beliefs entail.

Cortical columnar processing in the rat whisker-to-barrel system.

Controlled whisker stimulation and single-unit recordings were used to elucidate response transformations that occur during the processing of tactile information from ventral posterior medial thalamus (VPM) through cortical columns in the rat whisker/barrel cortex. Whiskers were either deflected alone, using punctate ramp-and-hold stimuli, or in combination with a random noise vibration applied simultaneously to two or more neighboring whiskers. Quantitative data were obtained from five anatomically defined groups of neurons based on their being located in: VPM, layer IV barrels, layer IV septa, supragranular laminae, and infragranular laminae. Neurons in each of these populations displayed characteristic properties related to their response latency and time course, relative magnitudes of responses evoked by stimulus onset versus offset, strength of excitatory responses evoked by the noise stimulus, and/or the degree to which the noise stimulus, when applied to neighboring whiskers, suppressed or facilitated responses evoked by the columnar whisker. Results indicate that within layer IV itself there are at least two anatomically distinct networks, barrel and septum, that independently process afferent information, transforming thalamic input in similar but quantitatively distinguishable ways. Transformed signals are passed on to circuits in supragranular and infragranular laminae. In the case of supragranular neurons, evidence suggests that circuits there function in a qualitatively different fashion from those in layer IV, diminishing response differentials between weak and strong inputs, rather than enhancing them. Compared to layer IV, the greater heterogeneity of receptive field properties in nongranular layers suggests the existence of multiple, operationally distinct local circuits in the output layers of the cortical column.

Sensory loss by selected whisker removal produces immediate disinhibition in the somatosensory cortex of behaving rats.

This study used extracellular unit recordings in behaving animals to evaluate thalamocortical response transformations in the rat whisker-barrel system. Based on previous acute studies using controlled whisker stimulation, we hypothesized that in a cortical barrel adjacent (non-principal) whiskers exert a net inhibitory effect. In contrast, in thalamic barreloid neurons, the effects of neighboring whiskers should be net facilitatory. We evaluated these hypotheses by recording unit activity at 21 sites in 17 animals trained to explore a wire mesh screen with their whiskers. In the middle of the recording session, selected vibrissae were clipped close to the skin surface. The absence of whiskers surrounding the principal whisker was associated with a mean 20% increase in cortical activity and, conversely, a 37% decrease in the thalamic activity. Removal of the principal whisker resulted in a 50% decrease in cortical unit firing. Findings are consistent with the idea that, in the behaving animal, each barrel uses multi-whisker thalamic inputs and local inhibitory circuitry to sharpen the receptive field properties of its constituent neurons. Cortical disinhibition as a consequence of selective whisker removal is likely to be an important factor underlying altered receptive field properties in sensory-deprived animals.

Functional independence of layer IV barrels in rodent somatosensory cortex.

Layer IV of rodent primary somatosensory cortex is characterized by an array of whisker-related groups of neurons, known as "barrels." Neurons within each barrel respond best to a particular whisker on the contralateral face, and, on deflection of adjacent whiskers, display relatively weak excitation followed by strong inhibition. A prominent hypothesis for the processing of vibrissal information within layer IV is that the multiwhisker receptive fields of barrel neurons reflect interconnections among neighboring barrels. An alternative view is that the receptive field properties of barrel neurons are derived from operations performed on multiwhisker, thalamic inputs by local circuitry within each barrel, independently of neighboring barrels. Here we report that adjacent whisker-evoked excitation and inhibition within a barrel are unaffected by ablation of the corresponding adjacent barrel. In supragranular neurons, on the other hand, excitatory responses to the ablated barrel's associated whisker are substantially reduced. We conclude that the layer IV barrels function as an array of independent parallel processors, each of which individually transforms thalamic afferent input for subsequent processing by horizontally interconnected circuits in other layers.

Active and passive scene recognition across views.

Recent evidence suggests that scene recognition across views is impaired when an array of objects rotates relative to a stationary observer, but not when the observer moves relative to a stationary display [Simons, D.J., Wang, R.F., 1998. Perceiving real-world viewpoint changes. Psychological Science 9, 315-320]. The experiments in this report examine whether the relatively poorer performance by stationary observers across view changes results from a lack of perceptual information for the rotation or from the lack of active control of the perspective change, both of which are present for viewpoint changes. Three experiments compared performance when observers passively experienced the view change and when they actively caused the change. Even with visual information and active control over the display rotation, change detection performance was still worse for orientation changes than for viewpoint changes. These findings suggest that observers can update a viewer-centered representation of a scene when they move to a different viewing position, but such updating does not occur during display rotations even with visual and motor information for the magnitude of the change. This experimental approach, using arrays of real objects rather than computer displays of isolated individual objects, can shed light on mechanisms that allow accurate recognition despite changes in the observer's position and orientation.

Gorillas in our midst: sustained inattentional blindness for dynamic events.

With each eye fixation, we experience a richly detailed visual world. Yet recent work on visual integration and change direction reveals that we are surprisingly unaware of the details of our environment from one view to the next: we often do not detect large changes to objects and scenes ('change blindness'). Furthermore, without attention, we may not even perceive objects ('inattentional blindness'). Taken together, these findings suggest that we perceive and remember only those objects and details that receive focused attention. In this paper, we briefly review and discuss evidence for these cognitive forms of 'blindness'. We then present a new study that builds on classic studies of divided visual attention to examine inattentional blindness for complex objects and events in dynamic scenes. Our results suggest that the likelihood of noticing an unexpected object depends on the similarity of that object to other objects in the display and on how difficult the priming monitoring task is. Interestingly, spatial proximity of the critical unattended object to attended locations does not appear to affect detection, suggesting that observers attend to objects and events, not spatial positions. We discuss the implications of these results for visual representations and awareness of our visual environment.

Laminar differences in bicuculline methiodide's effects on cortical neurons in the rat whisker/barrel system.

Extracellular unit recordings were made at various depths within SmI barrel cortex of immobilized, sedated rats, in the presence and absence of titrated amounts of the GABA(A) receptor antagonist bicuculline methiodide (BMI). Principal and adjacent whiskers were moved singly, or in paired combination in a condition-test paradigm, to assess excitatory and inhibitory receptive field (RF) characteristics. Neurons were classified as regular- or fast-spike units, and divided into three laminar groups: supragranular, granular (barrel), and infragranular. BMI increased response magnitude and duration, but did not affect response latencies. The excitatory RFs of barrel units, which are the most tightly focused on the principal whisker, were the most greatly defocused by BMI; infragranular units were least affected. All three layers had approximately equal amounts of adjacent whisker-evoked, surround inhibition, but BMI counteracted this inhibition substantially in barrel units and less so in infragranular units. The effects of BMI were most consistent in the barrel; more heterogeneity was found in the non-granular layers. These lamina-dependent effects of BMI are consistent with the idea that between-whisker inhibition is generated mostly within individual layer IV barrels as a result of the rapid engagement of strong, local inhibitory circuitry, and is subsequently embedded in layer IV's output to non-layer IV neurons. The latter's surround inhibition is thus relatively resistant to antagonism by locally applied BMI. The greater heterogeneity of non-granular units in terms of RF properties and the effects of BMI is consistent with other findings demonstrating that neighboring neurons in these layers may participate in different local circuits.

Thalamic relay of afferent responses to 1- to 12-Hz whisker stimulation in the rat.

Somatosensory cortical neurons in the rat can be entrained to frequencies of pulsatile whisker stimulation up to at least 12 Hz. A recent study proposed that such entrainment depends on oscillatory corticothalamic feedback. According to this model, thalamic relay neurons function as comparators of ascending and descending signals and should vary their response magnitudes and latencies as a function of peripheral stimulation frequency. Here we report, however, that the responses of thalamic relay neurons to 1- to 12-Hz pulsatile whisker deflections are constant in magnitude and latency over these frequencies. In addition, their cycle-by-cycle responses are as invariant as those of primary afferent neurons. These results support the view that thalamic relay neurons are driven primarily by ascending afferent signals and thereby entrain cortical neurons to peripheral stimulation by means of a direct feed-forward mechanism.

Two dogmas of conceptual empiricism: implications for hybrid models of the structure of knowledge.

Concepts seem to consist of both an associative component based on tabulations of feature typicality and similarity judgments and an explanatory component based on rules and causal principles. However, there is much controversy about how each component functions in concept acquisition and use. Here we consider two assumptions, or dogmas, that embody this controversy and underlie much of the current cognitive science research on concepts. Dogma 1: Novel information is first processed via similarity judgments and only later is influenced by explanatory components. Dogma 2: Children initially have only a similarity-based component for learning concepts; the explanatory component develops on the foundation of this earlier component. We present both empirical and theoretical arguments that these dogmas are unfounded, particularly with respect to real world concepts; we contend that the dogmas arise from a particular species of empiricism that inhibits progress in the study of conceptual structure; and finally, we advocate the retention of a hybrid model of the structure of knowledge despite our rejection of these dogmas.