scholarly journals Differential rapid plasticity in auditory and visual responses in the primarily multisensory orbitofrontal cortex

2019 ◽  
Author(s):  
Sudha Sharma ◽  
Sharba Bandyopadhyay

AbstractIn a dynamic environment with rapidly changing contingencies, the orbitofrontal cortex (OFC) guides flexible behavior through coding of stimulus value. Although stimulus-evoked responses in the OFC are known to convey outcome, baseline sensory response properties in the mouse OFC are poorly understood. To understand mechanisms involved in stimulus value/outcome encoding it is important to know the response properties of single neurons in the mouse OFC, purely from a sensory perspective. Ruling out effects of behavioral state, memory and others, we studied the anesthetized mouse OFC responses to auditory, visual and audiovisual/multisensory stimuli, multisensory associations and sensory-driven input organization to the OFC. Almost all, OFC single neurons were found to be multisensory in nature, with sublinear to supralinear integration of the component unisensory stimuli. With a novel multisensory oddball stimulus set, we show that the OFC receives both unisensory as well as multisensory inputs, further corroborated by retrograde tracers showing labeling in secondary auditory and visual cortices, which we find to also have similar multisensory integration and responses. With long audiovisual pairing/association, we show rapid plasticity in OFC single neurons, with a strong visual bias, leading to a strong depression of auditory responses and effective enhancement of visual responses. Such rapid multisensory association driven plasticity is absent in the auditory and visual cortices, suggesting its emergence in the OFC. Based on the above results we propose a hypothetical local circuit model in the OFC that integrates auditory and visual information which participates in computing stimulus value in dynamic multisensory environments.Significance StatementProperties and modification of sensory responses of neurons in the orbitofrontal cortex (OFC) involved in flexible behavior through stimulus value/outcome encoding are poorly understood. Such responses are critical in providing the framework for the encoding of stimulus value based on behavioral context while also directing plastic changes in sensory regions. The mouse OFC is found to be primarily multisensory with varied nonlinear interactions, explained by unisensory and multisensory inputs. Audio-visual associations cause rapid plastic changes in the OFC, which bias visual responses while suppressing auditory responses. Similar plasticity was absent in the sensory cortex. Thus the observed intrinsic visual bias in the OFC weighs visual stimuli more than associated auditory stimuli in value encoding in a dynamic multisensory environment.

2020 ◽  
Author(s):  
Hemant K Srivastava ◽  
Sharba Bandyopadhyay

AbstractThe orbitofrontal cortex (OFC), controls flexible behavior through stimulus value updating based on stimulus outcome associations, allowing seamless navigation in dynamic sensory environments with changing contingencies. Sensory cue driven responses, primarily studied through behavior, exist in the OFC. However, OFC neurons’ sensory response properties, particularly auditory, are unknown, in the mouse, a genetically tractable animal. We show that mouse OFC single neurons have unique auditory response properties showing pure deviance detection and long timescales of adaptation resulting in stimulus-history dependence. Further, we show that OFC auditory responses are shaped by two parallel sources in the auditory thalamus, lemniscal and non-lemniscal. The latter underlies a large component of the observed deviance detection and additionally controls persistent activity in the OFC through the amygdala. The deviant selectivity can serve as a signal for important changes in the auditory environment. Such signals if coupled with persistent activity, obtained by disinhibitory control from the non-lemniscal auditory thalamus or the amygdala, will allow for associations with a delayed outcome related signal, like reward prediction error, and potentially forms the basis of updating stimulus outcome associations in the OFC. Thus the baseline sensory responses allow the behavioral requirement based response modification through relevant inputs from other structures related to reward, punishment, or memory. Thus, alterations in these responses in neurological disorders can lead to behavioral deficits.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Sean E Cavanagh ◽  
Joni D Wallis ◽  
Steven W Kennerley ◽  
Laurence T Hunt

Correlates of value are routinely observed in the prefrontal cortex (PFC) during reward-guided decision making. In previous work (Hunt et al., 2015), we argued that PFC correlates of chosen value are a consequence of varying rates of a dynamical evidence accumulation process. Yet within PFC, there is substantial variability in chosen value correlates across individual neurons. Here we show that this variability is explained by neurons having different temporal receptive fields of integration, indexed by examining neuronal spike rate autocorrelation structure whilst at rest. We find that neurons with protracted resting temporal receptive fields exhibit stronger chosen value correlates during choice. Within orbitofrontal cortex, these neurons also sustain coding of chosen value from choice through the delivery of reward, providing a potential neural mechanism for maintaining predictions and updating stored values during learning. These findings reveal that within PFC, variability in temporal specialisation across neurons predicts involvement in specific decision-making computations.


1995 ◽  
Vol 74 (2) ◽  
pp. 751-762 ◽  
Author(s):  
G. Schoenbaum ◽  
H. Eichenbaum

1. Neural activity was recorded from the orbitofrontal cortex (OF) of rats performing an eight-odor discrimination task that included predictable associations between particular odor pairs. A modified linear discriminant analysis was employed to characterize the population response in each trial of the task as a point in an N-dimensional activity space with the firing rate of each cell in the population represented on one of the N dimensions. The ability of the ensemble to discriminate among conditions of a variable was reflected in the tendency of population responses to cluster together in this activity space for repetitions of a given condition. We assessed coding of several variables describing the period of odor sampling, focusing on aspects of current, past, and future events reflected in single-neuron firing patterns, in ensembles composed of 22-138 cells active during the period when the rats sampled the discriminative stimulus in each trial. 2. OF ensembles performed well at discriminating variables with relevance to task demands represented in single-neuron firing patterns, specifically the physical attributes and assigned reward contingency of the current odor as well as the expectation of reward in the following trial that could be inferred from the predictable associations between particular pairs of odors. OF ensembles were able to correctly identify the identity and assigned reward contingency of the current odor in up to 52% (chance = 12.5%) and 99% (chance = 50%) of all trials, respectively, such that the observed behavioral performance required a population of 5,364 odor-responsive cells in the case of odor identity and only 40 cells in the case of valence. Expectations regarding upcoming rewards based on both assigned response contingency and associations between particular pairs of odors were correctly classified in up to 67% (chance = 20%) of all trials such that the observed level of behavioral performance required a population of 3,169 cells. 3. Other information represented in the single-neuron firing patterns, such as the identity and reward contingency of the preceding odor and specific odor-odor associations, was poorly encoded by OF ensembles. Thus neural ensembles in OF may represent only some of the information reflected in single-neuron activity. Stable coding of only the most useful and relevant information by the ensemble might emerge from the tuning properties of single neurons under the influence of the task at hand, producing in the well-trained animal the observed pattern of broad and diverse coding by single neurons and selective, task-relevant coding by neural ensembles in OF.


10.1038/78868 ◽  
2000 ◽  
Vol 3 (9) ◽  
pp. 946-953 ◽  
Author(s):  
Gabriel Kreiman ◽  
Christof Koch ◽  
Itzhak Fried

2020 ◽  
Vol 124 (2) ◽  
pp. 432-442
Author(s):  
Allison J. Murphy ◽  
J. Michael Hasse ◽  
Farran Briggs

Interest in visual system homologies across species has recently increased. Across species, retinas contain diverse retinal ganglion cells including cells with unusual visual response properties. It is unclear whether rare retinal ganglion cells in carnivores project to and drive similarly unique visual responses in the visual thalamus. We discovered a rare subpopulation of thalamic neurons defined by unique spike shape and visual response properties, suggesting that nonstandard visual computations are common to many species.


2014 ◽  
Vol 2014 ◽  
pp. 1-13 ◽  
Author(s):  
Wolfger von der Behrens

Tinnitus is one of the major audiological diseases, affecting a significant portion of the ageing society. Despite its huge personal and presumed economic impact there are only limited therapeutic options available. The reason for this deficiency lies in the very nature of the disease as it is deeply connected to elementary plasticity of auditory processing in the central nervous system. Understanding these mechanisms is essential for developing a therapy that reverses the plastic changes underlying the pathogenesis of tinnitus. This requires experiments that address individual neurons and small networks, something usually not feasible in human patients. However, in animals such invasive experiments on the level of single neurons with high spatial and temporal resolution are possible. Therefore, animal models are a very critical element in the combined efforts for engineering new therapies. This review provides an overview over the most important features of animal models of tinnitus: which laboratory species are suitable, how to induce tinnitus, and how to characterize the perceived tinnitus by behavioral means. In particular, these aspects of tinnitus animal models are discussed in the light of transferability to the human patients.


2012 ◽  
Vol 108 (3) ◽  
pp. 935-942 ◽  
Author(s):  
Jie Tang ◽  
Weiguo Yang ◽  
Nobuo Suga

The central auditory system consists of the lemniscal and nonlemniscal pathways or systems, which are anatomically and physiologically different from each other. In the thalamus, the ventral division of the medial geniculate body (MGBv) belongs to the lemniscal system, whereas its medial (MGBm) and dorsal (MGBd) divisions belong to the nonlemniscal system. Lemniscal neurons are sharply frequency-tuned and provide highly frequency-specific information to the primary auditory cortex (AI), whereas nonlemniscal neurons are generally broadly frequency-tuned and project widely to cortical auditory areas including AI. These two systems are presumably different not only in auditory signal processing, but also in eliciting cortical plastic changes. Electric stimulation of narrowly frequency-tuned MGBv neurons evokes the shift of the frequency-tuning curves of AI neurons toward the tuning curves of the stimulated MGBv neurons (tone-specific plasticity). In contrast, electric stimulation of broadly frequency-tuned MGBm neurons augments the auditory responses of AI neurons and broadens their frequency-tuning curves (nonspecific plasticity). In our current studies, we found that electric stimulation of AI evoked tone-specific plastic changes of the MGBv neurons, whereas it degraded the frequency tuning of MGBm neurons by inhibiting their auditory responses. AI apparently modulates the lemniscal and nonlemniscal thalamic neurons in quite different ways. High MGBm activity presumably makes AI neurons less favorable for fine auditory signal processing, whereas high MGBv activity makes AI neurons more suitable for fine processing of specific auditory signals and reduces MGBm activity.


2019 ◽  
Author(s):  
Luciana López-Jury ◽  
Adrian Mannel ◽  
Francisco Garcia-Rosales ◽  
Julio C. Hechavarria

AbstractFrontal areas of the mammalian cortex are thought to be important for cognitive control and complex behaviour. These areas have been studied mostly in humans, non-human primates and rodents. In this article, we present a quantitative characterization of response properties of a frontal auditory area responsive to sound in the bat brain, the frontal auditory field (FAF). Bats are highly vocal animals and they constitute an important experimental model for studying the auditory system. At present, little is known about neuronal sound processing in the bat FAF. We combined electrophysiology experiments and computational simulations to compare the response properties of auditory neurons found in the bat FAF and auditory cortex (AC) to simple sounds (pure tones). Anatomical studies have shown that the latter provide feedforward inputs to the former. Our results show that bat FAF neurons are responsive to sounds, however, when compared to AC neurons, they presented sparser, less precise spiking and longer-lasting responses. Based on the results of an integrate-and-fire neuronal model, we speculate that slow, low-threshold, synaptic dynamics could contribute to the changes in activity pattern that occur as information travels through cortico-cortical projections from the AC to the FAF.


2017 ◽  
Author(s):  
Amelia J. Christensen ◽  
Jonathan W. Pillow

Running profoundly alters stimulus-response properties in mouse primary visual cortex (V1), but its effects in higher-order visual cortex remain unknown. Here we systematically investigated how locomotion modulates visual responses across six visual areas and three cortical layers using a massive dataset from the Allen Brain Institute. Although running has been shown to increase firing in V1, we found that it suppressed firing in higher-order visual areas. Despite this reduction in gain, visual responses during running could be decoded more accurately than visual responses during stationary periods. We show that this effect was not attributable to changes in noise correlations, and propose that it instead arises from increased reliability of single neuron responses during running.


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