Spiking History Shapes Dynamic Encoding of Polarization Angles in Central Complex Neurons of Bumblebees

核心概念

Spiking history of polarization-sensitive neurons in the central complex of bumblebees facilitates faster responses to dynamic changes in polarization angles and reduces overall energy consumption during straight flight.

摘要

The study investigated the dynamic response properties of polarization-sensitive neurons in the central complex of bumblebees. The researchers performed intracellular recordings and stimulated the neurons with naturalistic polarized-light stimuli that simulated the perception of free-flying bumblebees.
Key highlights:

Polarization-sensitive neurons in the central complex responded reliably across a wide range of rotation velocities, from 30°/s to 1920°/s, spanning the natural range of head rotations during flight.
The neurons' responses showed a dependency on spiking history, with increased activity after inhibition and decreased activity after excitation.
A computational model incorporating spiking history effects showed two main benefits:

It facilitates faster responses to changes in polarization angles during highly dynamic flight maneuvers.
It reduces overall population activity during straight flight, potentially conserving energy.

The model also showed that spiking history can lead to the population activity changing faster than the actual stimulus, potentially allowing the bees to anticipate future head directions and compensate for their moment of inertia.
The findings suggest that the spiking history-dependent properties of central complex neurons enable a flexible and efficient encoding of polarization angles to support the bees' spatial orientation during natural flight behaviors.

統計資料

"Depending on rotation velocity between 50% and 93.8% of the responses were significantly phase-locked to the stimulus."
"The average spiking rate during stimulation with a constantly rotating polarizer was correlated with the rotation velocity, peaking at 60°/s and continuously decreasing towards higher velocities."
"The median deviation between modelled and measured preferred angle of polarization was between 10.93° and 16.93° at lower and medium high rotation velocities (30°/s-240°/s)."
"The median ratio between the population vector average (PVA) velocity and the stimulus velocity was significantly elevated to 1.17 for saccades that occurred after at least 200 ms of stationary polarization input, compared to 1.02 for other saccades."

引述

"Spiking history has a directly impact on the overall population activity, which has two effects: First, it facilitates faster responses to stimulus changes during highly dynamic flight maneuvers, and increases sensitivity for course deviations during straight flight. Second, population activity during phases of constant polarization input is reduced, which might conserve energy during straight flight."

從以下內容提煉的關鍵洞見

History-dependent spiking facilitates efficient encoding of polarization angles in neurons of the central complex

by Roth... 於 www.biorxiv.org 07-26-2024

https://www.biorxiv.org/content/10.1101/2024.07.25.605186v1

深入探究

How do the spiking history-dependent properties of central complex neurons compare to other brain regions involved in spatial orientation, such as the hippocampus or entorhinal cortex in mammals?

The spiking history-dependent properties of central complex (CX) neurons in insects exhibit intriguing parallels and contrasts with similar mechanisms observed in mammalian brain regions such as the hippocampus and entorhinal cortex, both of which are critical for spatial orientation and navigation. In the CX, the study highlights how spiking history influences neuronal responses to polarized light, allowing for faster adjustments to heading signals and reduced overall activity during straight flight. This dynamic response is particularly beneficial for navigating complex environments, as it enables the encoding of rapidly changing spatial information.
In the hippocampus, place cells demonstrate a form of spiking history dependence, where the firing rate of these neurons is influenced by the animal's previous experiences and spatial context. This allows for the encoding of spatial memory and navigation through a learned environment. Similarly, entorhinal grid cells exhibit a form of temporal coding that can be influenced by the animal's movement history, providing a metric for spatial navigation. However, while both the CX and mammalian systems utilize spiking history to enhance spatial encoding, the mechanisms may differ. The CX neurons' responses are closely tied to the dynamics of polarized light stimuli, reflecting the immediate environmental context, whereas hippocampal and entorhinal neurons often integrate longer-term spatial experiences and contextual information.
Overall, while both systems exhibit spiking history-dependent properties that enhance spatial orientation, the specific mechanisms and the types of information encoded may vary significantly, reflecting the evolutionary adaptations of these neural circuits to their respective ecological niches.

What are the potential limitations of the computational model in capturing the full complexity of the neuronal dynamics and population coding in the central complex?

The computational model developed to simulate the spiking activity of polarization-sensitive neurons in the central complex has several limitations that may hinder its ability to fully capture the complexity of neuronal dynamics and population coding. Firstly, the model primarily focuses on a rate-code approach, which simplifies the intricate temporal dynamics of neuronal firing. This reduction may overlook important aspects of spike timing and the precise temporal patterns that can convey additional information about the stimulus.
Secondly, the model assumes a homogeneous population of neurons with similar parameters, which may not accurately reflect the diversity of neuronal types and their distinct tuning properties within the central complex. In reality, the CX comprises various neuron subtypes, each with unique response characteristics and connectivity patterns, which could significantly influence population coding and dynamics.
Additionally, the model's reliance on averaged parameters from a limited number of recordings may not account for individual variability among neurons. This could lead to oversimplifications in how the model predicts population responses to naturalistic stimuli. Furthermore, the model does not incorporate potential plasticity and adaptation mechanisms that may occur within the neuronal network over time, which could affect how neurons respond to repeated stimuli.
Lastly, while the model includes spiking history effects, it may not fully capture the underlying biological mechanisms that contribute to these effects, such as synaptic plasticity or adaptation at the receptor level. As a result, the model may provide a useful framework for understanding basic dynamics but may fall short in representing the full complexity of neuronal interactions and the rich behavioral implications of these dynamics in the central complex.

Could the principles of spiking history-dependent encoding discovered in this study on polarization-sensitive neurons be extended to other sensory modalities and brain regions involved in spatial navigation and decision-making?

The principles of spiking history-dependent encoding observed in polarization-sensitive neurons of the central complex have the potential to be extended to other sensory modalities and brain regions involved in spatial navigation and decision-making. This concept of spiking history influencing neuronal responses is not unique to the CX; it is likely a widespread phenomenon across various neural circuits.
In other sensory modalities, such as auditory or visual processing, neurons often exhibit adaptive responses based on previous stimuli. For instance, in the visual cortex, neurons can show changes in firing rates based on the history of visual stimuli, which can enhance contrast sensitivity and improve object recognition. Similarly, in the auditory system, neurons may adjust their responses based on the temporal patterns of sound, allowing for better discrimination of complex auditory scenes.
Moreover, in brain regions involved in spatial navigation, such as the hippocampus and entorhinal cortex, spiking history can play a crucial role in encoding spatial memories and navigating through environments. The ability of neurons to adjust their firing based on past experiences can enhance the encoding of spatial information, allowing for more efficient navigation and decision-making.
Extending these principles to decision-making processes, spiking history-dependent encoding could facilitate adaptive behavior by allowing neural circuits to integrate past experiences and current sensory inputs. This could lead to more flexible and context-sensitive decision-making, as observed in various cognitive tasks.
In summary, the principles of spiking history-dependent encoding discovered in the study of polarization-sensitive neurons in the central complex are likely applicable to a broader range of sensory modalities and brain regions. This suggests a fundamental mechanism by which neural circuits can dynamically adjust their responses based on both current stimuli and past experiences, enhancing the organism's ability to navigate and make decisions in complex environments.