Department of Physiology, McGill University, Montreal, QC, Canada.
Neuroscience. 2011 Jan 13;172:270-84. doi: 10.1016/j.neuroscience.2010.10.061. Epub 2010 Oct 28.
Peripheral sensory neurons respond to stimuli containing a wide range of spatio-temporal frequencies. We investigated electroreceptor neuron coding in the gymnotiform wave-type weakly electric fish Apteronotus leptorhynchus. Previous studies used low to mid temporal frequencies (<256 Hz) and showed that electroreceptor neuron responses to sensory stimuli could be almost exclusively accounted for by linear models, thereby implying a rate code. We instead used temporal frequencies up to 425 Hz, which is in the upper behaviorally relevant range for this species. We show that electroreceptors can: (A) respond up to the highest frequencies tested and (B) display strong nonlinearities in their responses to such stimuli. These nonlinearities were manifested by the fact that the responses to repeated presentations of the same stimulus were coherent at temporal frequencies outside of those contained in the stimulus waveform. Specifically, these consisted of low frequencies corresponding to the time varying contrast or envelope of the stimulus as well as higher harmonics of the frequencies contained in the stimulus. Heterogeneities in the afferent population influenced nonlinear coding as afferents with the lowest baseline firing rates tended to display the strongest nonlinear responses. To understand the link between afferent heterogeneity and nonlinear responsiveness, we used a phenomenological mathematical model of electrosensory afferents. Varying a single parameter in the model was sufficient to account for the variability seen in our experimental data and yielded a prediction: nonlinear responses to the envelope and at higher harmonics are both due to afferents with lower baseline firing rates displaying greater degrees of rectification in their responses. This prediction was verified experimentally as we found that the coherence between the half-wave rectified stimulus and the response resembled the coherence between the responses to repeated presentations of the stimulus in our dataset. This result shows that rectification cannot only give rise to responses to low frequency envelopes but also at frequencies that are higher than those contained in the stimulus. The latter result implies that information is contained in the fine temporal structure of electroreceptor afferent spike trains. Our results show that heterogeneities in peripheral neuronal populations can have dramatic consequences on the nature of the neural code.
周围感觉神经元对包含广泛时空频率的刺激做出反应。我们研究了电感受神经元在电鳗型弱电鱼 Apteronotus leptorhynchus 中的编码。以前的研究使用的是中低时间频率（<256 Hz），并表明电感受神经元对感觉刺激的反应几乎可以完全用线性模型来解释，从而暗示了一种率码。我们使用的时间频率高达 425 Hz，这在该物种的行为相关范围内处于较高水平。我们表明，电感受器可以：（A）对测试的最高频率做出反应；（B）对这些刺激的反应表现出强烈的非线性。这些非线性表现为，对相同刺激的重复呈现的反应在包含在刺激波形之外的时间频率上是相干的。具体来说，这些反应包括与刺激的时变对比度或包络相对应的低频，以及刺激中包含的频率的更高谐波。传入群体的异质性影响非线性编码，因为基线发射率最低的传入神经往往表现出最强的非线性反应。为了理解传入神经异质性和非线性反应能力之间的联系，我们使用了一种电感受传入神经的现象学数学模型。在模型中改变单个参数足以解释我们实验数据中的可变性，并产生了一个预测：对包络和更高谐波的非线性反应都是由于基线发射率较低的传入神经在其反应中表现出更大程度的整流。该预测在实验中得到了验证，因为我们发现半波整流刺激和反应之间的相干性类似于我们数据集中介于刺激重复呈现之间的反应的相干性。这一结果表明，整流不仅可以产生对低频包络的反应，还可以产生高于刺激中包含的频率的反应。后一结果意味着信息包含在电感受传入神经冲动序列的精细时间结构中。我们的结果表明，周围神经元群体的异质性会对神经编码的性质产生巨大影响。
