Redundancy Circuits of the Commissural Pathways in Human and Rhesus Macaque Brains

It has been hypothesized that the human brain has traded redundancy for efficiency, but the structural existence has not been identified to examine this claim. Here, we report three redundancy circuits of the commissural pathways in primate brains, namely the orbitofrontal, temporal, and occipital redundancy circuits of the anterior commissure and corpus callosum. Each redundancy circuit has two distinctly separated routes connecting a common pair of cortical regions. We mapped their trajectories in human and rhesus macaque brains using individual and population-averaged tractography. The dissection results confirmed the existence of these redundancy circuits connecting the orbitofrontal lobe, amygdala, and visual cortex. The volume analysis showed a significant reduction in the orbitofrontal and occipital redundancy circuits of the human brain, whereas the temporal redundancy circuit had a substantial organizational difference between the human and rhesus macaque. Our overall findings suggest that the human brain is more efficient in the commissural pathway, as shown by the significantly reduced volume of the anterior commissure which serves as the backup connections for the corpus callosum. This reduction of the redundancy circuit may explain why humans are more vulnerable to psychiatric brain disorders stemming from the corpus callosum compared to non-human primates.SignificanceWe report and describe the connection routes of three redundancy circuits of the commissural pathways in human and rhesus macaque brains and compare their volumes. Our tractography and dissection studies confirmed that the human brain has smaller redundancy circuits. This is the first time such redundancy circuits of the commissural pathways have been identified, and their differences quantified in human and rhesus macaque to verify the redundancy-efficiency tradeoff hypothesis. The findings provide new insight into the topological organization of the human brain and may help understand the circuit mechanism of brain disorders involving these pathways.

Directional preference of otolith-related neurons in vestibular nucleus

Background: Due to the paired structure of two labyrinths, their neural communication is conducted through the interconnected commissural pathway. Using the tight link, the neural responding characteristics are formed in vestibular nucleus, and these responses are initially generated by the mechanical movement of the hair cells in the semicircular canals and otoliths. Although the mechanism to describe the neuronal responses to the head movements was evident, few direct experimental data were provided, especially the directional preference of otolith-related neurons as one of critical responses to elucidate the function of the neurons in vestibular nucleus (VN). Experimental Approach: The directional preference of otolith-related neurons was investigated in VN. Also, a chemically induced unilateral labyrinthectomy (UL) was performed to identify the origin of the directional preference. For the model evaluation, static and dynamic behavioral tests were performed. Following the evaluation, an extracellular neural activity was recorded for the neuronal responses to the horizontal head rotation and the linear head translation. Results: Seventy seven neuronal activities were recorded from thirty SD rats (270-450 g, male), and total population was divided into three groups; left UL (20), sham (35), right UL (22). Based on the directional preference, two sub-groups were again classified as contra- and ipsi-preferred neurons. There was no significance in the number of those sub-groups (contra-: 15/35, 43%; ipsi-: 20/35, 57%) in the sham (p=0.155). However, more ipsi-preferred neurons (19/22, 86%) were observed after right UL (p=6.056×10-5) while left UL caused more contra-preferred neurons (13/20, 65%) (p=0.058). In particular, the convergent neurons mainly led this biased difference in the population (ipsi-: 100% after right UL & contra-: 89% after left UL) (p<0.002). Conclusion: The directional preference was evenly maintained under a normal vestibular function, and its unilateral loss biased the directional preference of the neurons, depending on the side of lesion. Moreover, the dominance of the directional preference was mainly led by the convergent neurons which had the neural information related with head rotation and linear translation.

Directional preference of otolith-related neurons in vestibular nucleus

Background: Due to the paired structure of two labyrinths, their neural communication is conducted through the interconnected commissural pathway. Using the tight link, the neural responding characteristics are formed in vestibular nucleus, and these responses are initially generated by the mechanical movement of the hair cells in the semicircular canals and otoliths. Although the mechanism to describe the neuronal responses to the head movements was evident, few direct experimental data were provided, especially the directional preference of otolith-related neurons as one of critical responses to elucidate the function of the neurons in vestibular nucleus (VN).Experimental Approach: The directional preference of otolith-related neurons was investigated in VN. Also, a chemically induced unilateral labyrinthectomy (UL) was performed to identify the origin of the directional preference. For the model evaluation, static and dynamic behavioral tests were performed. Following the evaluation, an extracellular neural activity was recorded for the neuronal responses to the horizontal head rotation and the linear head translation.Results: Seventy seven neuronal activities were recorded from thirty SD rats (270-450 g, male), and total population was divided into three groups; left UL (20), sham (35), right UL (22). Based on the directional preference, two sub-groups were again classified as contra- and ipsi-preferred neurons. There was no significance in the number of those sub-groups (contra-: 15/35, 43%; ipsi-: 20/35, 57%) in the sham (p=0.155). However, more ipsi-preferred neurons (19/22, 86%) were observed after right UL (p=6.056×10-5) while left UL caused more contra-preferred neurons (13/20, 65%) (p=0.058). In particular, the convergent neurons mainly led this biased difference in the population (ipsi-: 100% after right UL & contra-: 89% after left UL) (p<0.002).Conclusion: The directional preference was evenly maintained under a normal vestibular function, and its unilateral loss biased the directional preference of the neurons, depending on the side of lesion. Moreover, the dominance of the directional preference was mainly led by the convergent neurons which had the neural information related with head rotation and linear translation.

Handedness and White Matter Networks

The development and persistence of laterality is a key feature of human motor behavior, with the asymmetry of hand use being the most prominent. The idea that asymmetrical functions of the hands reflect asymmetries in terms of structural and functional brain organization has been tested many times. However, despite advances in laterality research and increased understanding of this population-level bias, the neural basis of handedness remains elusive. Recent developments in diffusion magnetic resonance imaging enabled the exploration of lateralized motor behavior also in terms of white matter and connectional neuroanatomy. Despite incomplete and partly inconsistent evidence, structural connectivity of both intrahemispheric and interhemispheric white matter seems to differ between left and right-handers. Handedness was related to asymmetry of intrahemispheric pathways important for visuomotor and visuospatial processing (superior longitudinal fasciculus), but not to projection tracts supporting motor execution (corticospinal tract). Moreover, the interindividual variability of the main commissural pathway corpus callosum seems to be associated with handedness. The review highlights the importance of exploring new avenues for the study of handedness and presents the latest state of knowledge that can be used to guide future neuroscientific and genetic research.

Fear Conditioning Potentiates the Hippocampal CA1 Commissural Pathway In vivo and Increases Awake Phase Sleep

The hippocampus is essential for spatial learning and memory. To assess learning we used contextual fear conditioning (cFC), where animals learn to associate a place with aversive events such as foot-shocks. Candidate memory mechanisms for cFC are long-term potentiation and long-term depression, but there is little direct evidence of those mechanisms operating in the hippocampus in vivo following cFC. Also, little is known about the behavioral state changes induced by cFC. To address these shortcomings, we used motion tracking and recorded local field potentials in freely behaving mice by placing a stimulating electrode in the left dorsal CA1 region and positioning recording electrodes in the right dorsal CA1 region. Synaptic strength in the commissural pathway was monitored by measuring field excitatory postsynaptic potentials (fEPSPs) before and after cFC. After cFC, the commissural pathway’s synaptic strength was potentiated. Although recordings were conducted during the wake phase of the light/dark cycle, the mice slept more in the post-conditioning period than in the pre-conditioning period. Relative to awake periods, in non-rapid eye movement (NREM) sleep the fEPSPs were larger in both pre- and post-conditioning periods. Therefore, to avoid sleep-related fEPSP changes confounding the effects of cFC learning, we accounted for the effects of sleep and still found long-term potentiation of the commissural pathway, but no significant long-term depression. Synaptic strength changes were not found in the no-shock, control group that simply explored the fear-conditioning chamber, indicating that exploration of the novel place did not produce the measurable effects caused by cFC. These results show that following cFC, the CA1 commissural pathway is potentiated, likely contributing to the functional integration of the left and right hippocampi in fear memory consolidation. In addition, the cFC paradigm produces significant changes in an animal’s behavioral state, which are observable as proximal changes in sleep patterns.

Directional preference of otolith-related neurons in vestibular nucleus

Background: Due to the paired structure of two labyrinths at both sides of ear, their communication is conducted through the interconnected commissural pathway. The close interconnection produces the neural responding property in vestibular nucleus, and the mechanical movement of the hair cells mainly specifies the property. However, the mechanism to initiate the responding property was evident based on the structure, but few direct experimental data were provided to understand the responding property based on the structure.Experimental Approach: The directional preference was investigated, which was one of critical neural responding property to illustrate the functional structure. Also, a chemically induced unilateral labyrinthectomy (UL) was performed to emphasize the preference. For the model evaluation, static and dynamic behavioral tests were applied, and the results demonstrated a practical model construction. Following the evaluation, an extracellular neural activity was conducted for the neuronal responses to the horizontal head rotation and the linear head movement.Results: Seventy seven neuronal activities were recorded from thirty SD rats (270-450 g, male), and total population was divided into three groups; left UL (20), sham (35), right UL (22). Based on the directional preference, two sub-groups were again classified as contra- and ipsi-preferred neurons. There was no significance between those sub-groups (contra-: 15/35, 43%; ipsi-: 20/35, 57%) in sham model. However, more ipsi-preferred neurons (19/22, 86%) were observed after right UL while left UL caused more contra-preferred neurons (13/20, 65%). In particular, the convergent neurons mainly led this biased difference in the population (ipsi-: 100% after right UL & contra-: 89% after left UL).Conclusion: The directional preference was evenly maintained under a normal vestibular function, and its unilateral loss biased the directional preference of the neurons, depending on the side of lesion. Moreover, the dominance of the directional preference was mainly led by the convergent neurons which had the neural information related with head rotation and linear translation.

Encoding of Eye Position in the Goldfish Horizontal Oculomotor Neural Integrator

Monocular organization of the goldfish horizontal neural integrator was studied during spontaneous scanning saccadic and fixation behaviors. Analysis of neuronal firing rates revealed a population of ipsilateral (37%), conjugate (59%), and contralateral (4%) eye position neurons. When monocular optokinetic stimuli were employed to maximize disjunctive horizontal eye movements, the sampled population changed to 57, 39, and 4%. Monocular eye tracking could be elicited at different gain and phase with the integrator time constant independently modified for each eye by either centripetal (leak) or centrifugal (instability) drifting visual stimuli. Acute midline separation between the hindbrain oculomotor integrators did not affect either monocularity or time constant tuning, corroborating that left and right eye positions are independently encoded within each integrator. Together these findings suggest that the “ipsilateral” and “conjugate/contralateral” integrator neurons primarily target abducens motoneurons and internuclear neurons, respectively. The commissural pathway is proposed to select the conjugate/contralateral eye position neurons and act as a feedfoward inhibition affecting null eye position, oculomotor range, and saccade pattern.