Dynamic shifts of visual receptive fields in cortical area MT by spatial attention

Voluntary attention is the top-down selection process that focuses cortical processing resources on the most relevant sensory information. Spatial attention--that is, selection based on stimulus position--alters neuronal responsiveness throughout primate visual cortex. It has been hypothesized that it also changes receptive field profiles by shifting their centers toward attended locations and by shrinking them around attended stimuli. Here we examined, at high resolution, receptive fields in cortical area MT of rhesus macaque monkeys when their attention was directed to different locations within and outside these receptive fields. We found a shift of receptive fields, even far from the current location of attention, accompanied by a small amount of shrinkage. Thus, already in early extrastriate cortex, receptive fields are not static entities but are highly modifiable, enabling the dynamic allocation of processing resources to attended locations and supporting enhanced perception within the focus of attention by effectively increasing the local cortical magnification.     

Alterations in visual receptive fields in the superior colliculus induced by amphetamine

Summary Visual response properties were examined in the superficial layers of the superior colliculus (SC) of anesthetized, paralyzed cats before and after i.v. administration of d-amphetamine. Receptive fields (RFs) of single SC units were plotted using small spots of light presented to the contralateral eye. Within the first hour following d-amphetamine injections, RF size gradually increased, reaching a maximum 86 min post-injection. On average, the area of the RF increased by 5.6 times and RF expansion was observed in all single units examined in the superficial layers. Over the subsequent 4–8 h following the injection, RF area gradually decreased and returned to control dimensions. Most RFs displayed asymmetrical patterns of expansion, showing relatively more horizontal than vertical growth. As RF expansion developed, responses to stimuli flashed on and off at various locations both inside and outside the borders of the control RF became progressively more vigorous. In contrast, no significant changes were noted in directionselective responses at any time after d-amphetamine injections. Using an array of light bar stimuli of different lengths, the strength of surround suppression was found to be significantly diminished by d-amphetamine. The reduction in surround suppression was especially clear for bar lengths which exceeded the diameter of the control RF. No RF expansion was observed in the superficial layers of the SC when d-amphetamine was injected intravitreally. Furthermore, d-amphetamine had no discernable effect on the RF sizes of cells in the visual cortex. These results suggest that the RF changes in the SC were not of either retinal or cortical origin. We conclude that the mean retinal area which can potentially influence the activity of RFs in the superficial layers of the SC may be on average over 5 times greater than the RF area determined using conventional methods and criteria. These findings raise the interesting possibility that the relatively small size and sharp borders characteristic of RFs in the superficial layers arise from local inhibitory networks which delimit a broader field of excitatory activity supplied by retinal and cortical afferent terminals. Thus, in order to generate the RF changes observed here, either these local inhibitory circuits are amphetamine sensitive, or more likely, these inhibitory networks are dynamically modulated by an, as yet unidentified, amphetamine-sensitive input affecting visual RFs in the superficial layers.     

Thalamocortical specificity and the synthesis of sensory cortical receptive fields

A persistent and fundamental question in sensory cortical physiology concerns the manner in which receptive fields of layer-4 neurons are synthesized from their thalamic inputs. According to a hierarchical model proposed more than 40 years ago, simple receptive fields in layer 4 of primary visual cortex originate from the convergence of highly specific thalamocortical inputs (e.g., geniculate inputs with on-center receptive fields overlap the on subregions of layer 4 simple cells). Here, we summarize studies in the visual cortex that provide support for this high specificity of thalamic input to visual cortical simple cells. In addition, we review studies of GABAergic interneurons in the somatosensory "barrel" cortex with receptive fields that are generated by a very different mechanism: the nonspecific convergence of thalamic inputs with different response properties. We hypothesize that these 2 modes of thalamocortical connectivity onto subpopulations of excitatory and inhibitory neurons constitute a general feature of sensory neocortex and account for much of the diversity seen in layer-4 receptive fields.     

Local signals from beyond the receptive fields of striate cortical neurons

We examined in anesthetized macaque how the responses of a striate cortical neuron to patterns inside the receptive field were altered by surrounding patterns outside it. The changes in a neuron's response brought about by a surround are immediate and transient: they arise with the same latency as the response to a stimulus within the receptive field (this argues for a source locally in striate cortex) and become less effective as soon as 27 ms later. Surround signals appeared to exert their influence through divisive interaction (normalization) with those arising in the receptive field. Surrounding patterns presented at orientations slightly oblique to the preferred orientation consistently deformed orientation tuning curves of complex (but not simple) cells, repelling the preferred orientation but without decreasing the discriminability of the preferred grating and ones at slightly oblique orientations. By reducing responsivity and changing the tuning of complex cells locally in stimulus space, surrounding patterns reduce the correlations among responses of neurons to a particular stimulus, thus reducing the redundancy of image representation.     

Spatio-temporal plasticity of cortical receptive fields in response to repetitive visual stimulation in the adult cat

Many psychophysical experiments on perceptual learning in humans show increases of performance that are most probably based on functions of early visual cortical areas. Long-term plasticity of the primary visual cortex has so far been shown in vivo with the use of visual stimuli paired with electrical or pharmacological stimulation at the cellular level. Here, we report that plasticity in the adult visual cortex can be achieved by repetitive visual stimulation. First, spatial receptive field profiles of single units (n=38) in area 17 or 18 of the anesthetized cat were determined with optimally oriented flashing light bars. Then a conditioning protocol was applied to induce associative synaptic plasticity. The receptive field center and an unresponsive region just outside the excitatory receptive field were synchronously stimulated ('costimulation', repetition rate 1 Hz; for 10-75 min). After costimulation the receptive field and its adjacent regions were mapped again. We observed specific increases of the receptive field size, changes of the receptive field subfield structure as well as shifts in response latency.In 37% of the cells the receptive field size increased specifically towards the stimulated side but not towards the non-stimulated opposite side of the receptive field. In addition, changes in the relative strength and size of the on and off subfield regions were observed. These specific alterations were dependent on the level of neuronal activity during costimulation. During recovery, the new responses dropped down to 120% of the preconditioning value on average within 103 min; however, the decay times significantly depended on the response magnitude after costimulation. In the temporal domain, the latency of new responses appeared to be strongly influenced by the latency of the response during costimulation.Twenty-nine percent of the units displayed no receptive field enlargement, most likely because the activity during costimulation was significantly lower than in the cases with enlarged receptive fields. An unspecific receptive field enlargement towards both the stimulated and non-stimulated side was observed in 34% of the tested cells. In contrast to the cells with specifically enlarged receptive fields, the unspecific increase of receptive field size was always accompanied by a strong increase of the general activity level.We conclude that the receptive field changes presumably took place by strengthening of synaptic inputs at the recorded cells in a Hebbian way as previously shown in the visual cortex in vitro and in vivo. The observed receptive field changes may be related to preattentive perceptual learning and could represent a basis of the 'filling in' of cortical scotomas obtained with specific training procedures in human patients suffering from visual cortex lesions.     

Multiparametric auditory receptive field organization across five cortical fields in the albino rat

The auditory cortex of the rat is becoming an increasingly popular model system for studies of experience-dependent receptive field plasticity. However, the relative position of various fields within the auditory core and the receptive field organization within each field have yet to be fully described in the normative case. In this study, the macro- and micro-organizational features of the auditory cortex were studied in pentobarbital-anesthetized adult rats with a combination of physiological and anatomical methods. Dense microelectrode mapping procedures were used to identify the relative position of five tonotopically organized fields within the auditory core: primary auditory cortex (AI), the posterior auditory field (PAF), the anterior auditory field (AAF), the ventral auditory field (VAF), and the suprarhinal auditory field (SRAF). AI and AAF both featured short-latency, sharply tuned responses with predominantly monotonic intensity-response functions. SRAF and PAF were both characterized by longer-latency, broadly tuned responses. VAF directly abutted the ventral boundary of AI but was almost exclusively composed of low-threshold nonmonotonic intensity-tuned responses. Dual injection of retrograde tracers into AI and VAF was used to demonstrate that the sources of thalamic input from the medial geniculate body to each area were essentially nonoverlapping. An analysis of receptive field parameters beyond characteristic frequency revealed independent spatially ordered representations for features related to spectral tuning, intensity tuning, and onset response properties in AI, AAF, VAF, and SRAF. These data demonstrate that despite its greatly reduced physical scale, the rat auditory cortex features a surprising degree of organizational complexity and detail.     

Spatiotemporal mechanisms in receptive fields of visual cortical simple cells: a model

1. Simple cells in the visual cortex have been subdivided into nondirection-selective (NDS), direction asymmetric (DA), and direction-selective (DS) cells. DA cells reverse their preferred direction with reversal of the stimulus contrast; DS2 cells respond with the same preferred direction for light and dark stimuli, whereas DS1 cells respond only to one (light or dark) contrast. Also, four velocity response groups have been distinguished: velocity broadband, low-pass, high-pass, and -tuned cells. This study describes an analytic model of feed-forward spatiotemporal interactions within a receptive field that reproduces these basic features of cortical simple cell behavior in the cat. 2. The spatial structure of the receptive fields is simulated with Gabor functions. Two neurobiologically plausible mechanisms, temporal low-pass filtering and intracortical spatial distribution of activity, are modeled. The central feature of the study is the implementation of both mechanisms in a spatially continuous way. The model is analytic, but an equivalent neural network diagram was drawn and is used to explain the features of the model. 3. First-order temporal low-pass filtering is performed both after convolving the stimulus light-intensity function with the Gabor type receptive field and also at the final output step of the model. In the circuit diagram this would correspond to low-pass filtering in lateral geniculate nucleus (LGN) and cortical cells. Filtering was adjusted to have a -3-dB drop-off frequency of 2-3 Hz, corresponding to the drop-off frequencies observed in response to temporal modulation of sine-wave gratings. 4. The mechanism that we call intracortical distribution of activity is implemented along the axis of stimulus motion. A response elicited from the part of the receptive field that is stimulated at a given time will spread out in the receptive field, influencing regions that have not been stimulated. It is equivalent to spreading of activity on the cortical surface. This mechanism extends the existing ideas of discrete interactions between subfields to a continuous scheme throughout the whole receptive field. It is based on findings that intracortical interactions exist even within single subfields. The impact of distributing the activity is assumed to decrease exponentially with the Euclidian distance between the stimulated region and the region under consideration. 5. Thresholds are implemented only at the level of the cortex. Both the activity distributing mechanism and the output of the cell being studied are thresholded.(ABSTRACT TRUNCATED AT 400 WORDS)     

Spatiotemporal architecture of cortical receptive fields and its impact on multisensory interactions

Recent electrophysiology studies have suggested that neuronal responses to multisensory stimuli may possess a unique temporal signature. To evaluate this temporal dynamism, unisensory and multisensory spatiotemporal receptive fields (STRFs) of neurons in the cortex of the cat anterior ectosylvian sulcus were constructed. Analyses revealed that the multisensory STRFs of these neurons differed significantly from the component unisensory STRFs and their linear summation. Most notably, multisensory responses were found to have higher peak firing rates, shorter response latencies, and longer discharge durations. More importantly, multisensory STRFs were characterized by two distinct temporal phases of enhanced integration that reflected the shorter response latencies and longer discharge durations. These findings further our understanding of the temporal architecture of cortical multisensory processing, and thus provide important insights into the possible functional role(s) played by multisensory cortex in spatially directed perceptual processes.     

Quantification of excitatory receptive fields of complex neurones in cat striate cortex

To use sensory information from the skin to guide motor behaviour the central nervous system must transform sensory coordinates into movement coordinates. As yet, the basic principles of this crucial neural computation are unclear. One motor system suitable as a model for the study of such transformations is the spinal withdrawal reflex system. The spatial organization of the cutaneous input to these reflexes has been characterized, and we now introduce a novel method of motion analysis permitting a quantitative analysis of the spatial input-output relationship in this motor system. For each muscle studied, a mirror-image relationship was found between the spatial distribution of reflex gain for cutaneous input and the pattern of cutaneous unloading ensuing on contraction. Thus, there is an imprint of the movement pattern on this motor system permitting effective sensorimotor transformation. This imprint may indicate the presence of a learning process which utilizes the sensory feedback ensuing on muscle contraction.     

Processing of low-probability sounds by cortical neurons

The ability to detect rare auditory events can be critical for survival. We report here that neurons in cat primary auditory cortex (A1) responded more strongly to a rarely presented sound than to the same sound when it was common. For the rare stimuli, we used both frequency and amplitude deviants. Moreover, some A1 neurons showed hyperacuity for frequency deviants--a frequency resolution one order of magnitude better than receptive field widths in A1. In contrast, auditory thalamic neurons were insensitive to the probability of frequency deviants. These phenomena resulted from stimulus-specific adaptation in A1, which may be a single-neuron correlate of an extensively studied cortical potential--mismatch negativity--that is evoked by rare sounds. Our results thus indicate that A1 neurons, in addition to processing the acoustic features of sounds, may also be involved in sensory memory and novelty detection.     

Periodic excitability changes across the receptive fields of complex cells in the striate and parastriate cortex of the cat.

1. Complex cells in cortical areas 17 and 18 of the cat have been studied in response to narrow slits and edges moving across the receptive field in the preferred direction and also to stationary slits of different widths. 2. Average response histograms, recorded as a narrow slit was moved across the receptive field, displayed a periodic series of peaks above a base line level. The response histogram for most area 17 and 18 cells contained five principal peaks; sometimes one or two weaker peaks were present at receptive field borders. The histogram for one cell located at the area 17-18 border showed thirteen distinct peaks. Periodic response patterns were also generated as an extended edge was moved across the receptive field. Plots of cell responses versus slit width for stationary slits of different widths also indicated periodic response pattern. 3. The accuracy of determining the preferred slit orientation was the single most important requirement for demonstrating the periodic response pattern. Significant changes in the appearance of the periodic pattern occurred even upon 5 degrees rotations away from the preferred orientation. 4. Average response histograms were also studied over a wide range of moving slit velocities. The number of peaks across corresponding spacings within the recewptive field remained constant over a range of velocities. Response amplitudes, however, were velocity dependent. Thus the response peaks remain associated with fixed positions within visual space independent of stimulus velocity, even though temporal as well as spatial factors may be involved in response selectivity and the periodic modulation. The most striking periodic response histograms were generated at the velocities which produced the greatest cell firing rates. Area 17 complex cells responded well to velocities of less than 0-5 degrees to 6-0 degrees/sec, but cells in area 18 generally required higher velocities, sometimes as high as 20 degrees--30 degrees/sec, for a good response. 5. Spatial frequencies for the periodic component of the receptive field for area 17 cells in the central visual area covered a range of three octaves up to 5 cycles/degree, and area 18 cells included another octave on the low frequency side. The spatial frequency of a cell was found to be roughly inversely proportional to the receptive field width. Only a small sample of area 18 cells was studied, but these cells tended to represent low spatial frequencies and to respond selectively to high velocity stimuli...