scholarly journals In monkeys making value-based decisions, amygdala neurons are sensitive to cue value as distinct from cue salience

2017 ◽  
Vol 117 (4) ◽  
pp. 1499-1511 ◽  
Author(s):  
Marvin L. Leathers ◽  
Carl R. Olson

Neurons in the lateral intraparietal (LIP) area of macaque monkey parietal cortex respond to cues predicting rewards and penalties of variable size in a manner that depends on the motivational salience of the predicted outcome (strong for both large reward and large penalty) rather than on its value (positive for large reward and negative for large penalty). This finding suggests that LIP mediates the capture of attention by salient events and does not encode value in the service of value-based decision making. It leaves open the question whether neurons elsewhere in the brain encode value in the identical task. To resolve this issue, we recorded neuronal activity in the amygdala in the context of the task employed in the LIP study. We found that responses to reward-predicting cues were similar between areas, with the majority of reward-sensitive neurons responding more strongly to cues that predicted large reward than to those that predicted small reward. Responses to penalty-predicting cues were, however, markedly different. In the amygdala, unlike LIP, few neurons were sensitive to penalty size, few penalty-sensitive neurons favored large over small penalty, and the dependence of firing rate on penalty size was negatively correlated with its dependence on reward size. These results indicate that amygdala neurons encoded cue value under circumstances in which LIP neurons exhibited sensitivity to motivational salience. However, the representation of negative value, as reflected in sensitivity to penalty size, was weaker than the representation of positive value, as reflected in sensitivity to reward size. NEW & NOTEWORTHY This is the first study to characterize amygdala neuronal responses to cues predicting rewards and penalties of variable size in monkeys making value-based choices. Manipulating reward and penalty size allowed distinguishing activity dependent on motivational salience from activity dependent on value. This approach revealed in a previous study that neurons of the lateral intraparietal (LIP) area encode motivational salience. Here, it reveals that amygdala neurons encode value. The results establish a sharp functional distinction between the two areas.

Science ◽  
2012 ◽  
Vol 338 (6103) ◽  
pp. 132-135 ◽  
Author(s):  
Marvin L. Leathers ◽  
Carl R. Olson

In monkeys deciding between alternative saccadic eye movements, lateral intraparietal (LIP) neurons representing each saccade fire at a rate proportional to the value of the reward expected upon its completion. This observation has been interpreted as indicating that LIP neurons encode saccadic value and that they mediate value-based decisions between saccades. Here, we show that LIP neurons representing a given saccade fire strongly not only if it will yield a large reward but also if it will incur a large penalty. This finding indicates that LIP neurons are sensitive to the motivational salience of cues. It is compatible neither with the idea that LIP neurons represent action value nor with the idea that value-based decisions take place in LIP neurons.


2005 ◽  
Vol 94 (2) ◽  
pp. 1469-1497 ◽  
Author(s):  
Matthew R. Roesch ◽  
Carl R. Olson

In macaque monkeys performing a memory-guided saccade task for a reward of variable size, neuronal activity in several areas of frontal cortex is stronger when the monkey anticipates a larger reward. This effect might depend on either the size or the value of the reward. To distinguish between these possibilities, we recorded from neurons in frontal cortex while controlling value through a manipulation of time rather than amount. A cue presented at the beginning of each trial, predicted the length of the delay during which the monkey would have to maintain fixation before performing a saccade and receiving a reward of fixed size. Predicting a short delay had effects closely similar to those of predicting a large reward: 1) monkeys were more motivated when working for a reward at short delay, 2) neurons tended to fire more strongly before a short delay, 3) individual neurons firing more strongly before a short delay tended also to fire more strongly before a large reward, and 4) the tendency to fire more strongly before a short delay was far more pronounced in premotor areas caudal to the arcuate sulcus than in association areas rostral to it. The association areas, in contrast, were marked by a tendency for neurons to fire more strongly at the end of the long delay. We conclude that predicting a short delay, like predicting a large reward, induces an enhancement of neuronal activity related to motivational modulation of the monkey's preparatory state.


Author(s):  
Sarah F. Beul ◽  
Alexandros Goulas ◽  
Claus C. Hilgetag

AbstractStructural connections between cortical areas form an intricate network with a high degree of specificity. Many aspects of this complex network organization in the adult mammalian cortex are captured by an architectonic type principle, which relates structural connections to the architectonic differentiation of brain regions. In particular, the laminar patterns of projection origins are a prominent feature of structural connections that varies in a graded manner with the relative architectonic differentiation of connected areas in the adult brain. Here we show that the architectonic type principle is already apparent for the laminar origins of cortico-cortical projections in the immature cortex of the macaque monkey. We find that prenatal and neonatal laminar patterns correlate with cortical architectonic differentiation, and that the relation of laminar patterns to architectonic differences between connected areas is not substantially altered by the complete loss of visual input. Moreover, we find that the degree of change in laminar patterns that projections undergo during development varies in proportion to the relative architectonic differentiation of the connected areas. Hence, it appears that initial biases in laminar projection patterns become progressively strengthened by later developmental processes. These findings suggest that early neurogenetic processes during the formation of the brain are sufficient to establish the characteristic laminar projection patterns. This conclusion is in line with previously suggested mechanistic explanations underlying the emergence of the architectonic type principle and provides further constraints for exploring the fundamental factors that shape structural connectivity in the mammalian brain.


2009 ◽  
Vol 101 (3) ◽  
pp. 1351-1360 ◽  
Author(s):  
Kumud K. Kunjilwar ◽  
Harvey M. Fishman ◽  
Dario J. Englot ◽  
Roger G. O'Neil ◽  
Edgar T. Walters

Learning and memory depend on neuronal alterations induced by electrical activity. Most examples of activity-dependent plasticity, as well as adaptive responses to neuronal injury, have been linked explicitly or implicitly to induction by Ca2+ signals produced by depolarization. Indeed, transient Ca2+ signals are commonly assumed to be the only effective transducers of depolarization into adaptive neuronal responses. Nevertheless, Ca2+-independent depolarization-induced signals might also trigger plastic changes. Establishing the existence of such signals is a challenge because procedures that eliminate Ca2+ transients also impair neuronal viability and tolerance to cellular stress. We have taken advantage of nociceptive sensory neurons in the marine snail Aplysia, which exhibit unusual tolerance to extreme reduction of extracellular and intracellular free Ca2+ levels. The axons of these neurons exhibit a depolarization-induced memory-like hyperexcitability that lasts a day or longer and depends on local protein synthesis for induction. Here we show that transient localized depolarization of these axons in an excised nerve–ganglion preparation or in dissociated cell culture can induce short- and intermediate-term axonal hyperexcitability as well as long-term protein synthesis–dependent hyperexcitability under conditions in which Ca2+ entry is prevented (by bathing in nominally Ca2+ -free solutions containing EGTA) and detectable Ca2+ transients are eliminated (by adding BAPTA-AM). Disruption of Ca2+ release from intracellular stores by pretreatment with thapsigargin also failed to affect induction of axonal hyperexcitability. These findings suggest that unrecognized Ca2+-independent signals exist that can transduce intense depolarization into adaptive cellular responses during neuronal injury, prolonged high-frequency activity, or other sustained depolarizing events.


2021 ◽  
Vol 17 (7) ◽  
pp. 1371-1379
Author(s):  
Di Liu ◽  
Ying Li ◽  
Jiechen Liu ◽  
Zhiyuan Shen ◽  
Fengying Wang ◽  
...  

Occlusal trauma (OT), by causing periodontal tissue damage, can activate and enhance the activity of the peripheral and central nervous system (CNS) neuropeptides. The brain-derived neurotrophic factor (BDNF) gene is activity-dependent and exhibits marked alterations, characterized by protection against injury and repair. Our results show the possible molecular mechanism through which noxious environmental stimuli induce alterations in BDNF activity in the local periodontal tissue, the primary sensory neurons-Vc, and the hippocampus, suggesting systemic impairment. BDNF serves a more positive and enduring trauma protection and repair function in Vc compared to that in local dental tissue.


2013 ◽  
Vol 109 (2) ◽  
pp. 518-545 ◽  
Author(s):  
K. P. Schultz ◽  
C. Busettini

Saccadic eye movements are rapid transfers of gaze between objects of interest. Their duration is too short for the visual system to be able to follow their progress in time. Adaptive mechanisms constantly recalibrate the saccadic responses by detecting how close the landings are to the selected targets. The double-step saccadic paradigm is a common method to simulate alterations in saccadic gain. While the subject is responding to a first target shift, a second shift is introduced in the middle of this movement, which masks it from visual detection. The error in landing introduced by the second shift is interpreted by the brain as an error in the programming of the initial response, with gradual gain changes aimed at compensating the apparent sensorimotor mismatch. A second shift applied dichoptically to only one eye introduces disconjugate landing errors between the two eyes. A monocular adaptive system would independently modify only the gain of the eye exposed to the second shift in order to reestablish binocular alignment. Our results support a binocular mechanism. A version-based saccadic adaptive process detects postsaccadic version errors and generates compensatory conjugate gain alterations. A vergence-based saccadic adaptive process detects postsaccadic disparity errors and generates corrective nonvisual disparity signals that are sent to the vergence system to regain binocularity. This results in striking dynamical similarities between visually driven combined saccade-vergence gaze transfers, where the disparity is given by the visual targets, and the double-step adaptive disconjugate responses, where an adaptive disparity signal is generated internally by the saccadic system.


1992 ◽  
Vol 67 (4) ◽  
pp. 961-980 ◽  
Author(s):  
J. J. Knierim ◽  
D. C. van Essen

1. We recorded responses from neurons in area V1 of the alert macaque monkey to textured patterns modeled after stimuli used in psychophysical experiments of pop-out. Neuronal responses to a single oriented line segment placed within a cell's classical receptive field (CRF) were compared with responses in which the center element was surrounded by rings of elements placed entirely outside the CRF. The orientations of the surround elements either matched the center element, were orthogonal to it, or were random. 2. The addition of the textured surround tended to suppress the response to the center element by an average of 34%. Overall, almost 80% of the 122 cells analyzed in detail were significantly suppressed by at least one of the texture surrounds. 3. Cells tended to respond more strongly to a stimulus in which there was a contrast in orientation between the center and surround than to a stimulus lacking such contrast. The average difference was 9% of the response to the optimally oriented center element alone. For the 32% of the cells showing a statistically significant orientation contrast effect, the average difference was 28%. 4. Both the general suppression and orientation contrast effects originated from surround regions at the ends of the center bar as well as regions along the sides of the center bar. 5. The amount of suppression induced by the texture surround decreased as the density of the texture elements decreased. 6. Both the general suppression and the orientation contrast effects appeared early in the population response to the stimuli. The general suppression effect took approximately 7 ms to develop, whereas the orientation contrast effect took 18-20 ms to develop. 7. These results are consistent with a possible functional role of V1 cells in the mediation of perceptual pop-out and in the segregation of texture borders. Possible anatomic substrates of the effects are discussed.


2011 ◽  
Vol 106 (4) ◽  
pp. 1862-1874 ◽  
Author(s):  
Jan Churan ◽  
Daniel Guitton ◽  
Christopher C. Pack

Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Arthur-Ervin Avramiea ◽  
Richard Hardstone ◽  
Jan-Matthis Lueckmann ◽  
Jan Bím ◽  
Huibert D Mansvelder ◽  
...  

Understanding why identical stimuli give differing neuronal responses and percepts is a central challenge in research on attention and consciousness. Ongoing oscillations reflect functional states that bias processing of incoming signals through amplitude and phase. It is not known, however, whether the effect of phase or amplitude on stimulus processing depends on the long-term global dynamics of the networks generating the oscillations. Here, we show, using a computational model, that the ability of networks to regulate stimulus response based on pre-stimulus activity requires near-critical dynamics—a dynamical state that emerges from networks with balanced excitation and inhibition, and that is characterized by scale-free fluctuations. We also find that networks exhibiting critical oscillations produce differing responses to the largest range of stimulus intensities. Thus, the brain may bring its dynamics close to the critical state whenever such network versatility is required.


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