Effects of low frequency electric fields on synaptic integration in hippocampal CA1 pyramidal neurons: implications for power line emissions

Abstract

The possible cognitive effects of low frequency external electric fields (EFs), such as those generated by power lines, are poorly understood. Their functional consequences for mechanisms at the single neuron level are very difficult to study and identify experimentally, especially in vivo. The major open problem is that experimental investigations on humans have given inconsistent or contradictory results, making it difficult to estimate the possible effects of external low frequency electric fields on cognitive functions. Here we investigate this issue with realistic models of hippocampal CA1 pyramidal neurons. Our findings suggest how and why EFs, with environmentally observed frequencies and intensities far lower than what is required for direct neural activation, can perturb dendritic signal processing and somatic firing of neurons that are crucially involved in cognitive tasks such as learning and memory. These results show that individual neuronal morphology, ion channel dendritic distribution, and alignment with the electric field are major determinants of overall effects, and provide a physiologically plausible explanation of why experimental findings can appear to be small and difficult to reproduce, yet deserve serious consideration.

The possible consequences for cognitive functions of external electric fields at power line frequency on hippocampal CA1 pyramidal neurons

“…As previously noted (Cavarretta et al ., ), and confirmed in this work, individual neurons in their specific and instantaneous absolute spatial location can interact with an EF in completely different ways. Their firing rate and timing can be just unaffected or significantly altered.…”

“…In agreement with previous publications (Ozen et al ., ; Berzhanskaya et al ., ; Cavarretta et al ., ), this result suggests that the presence of an EF oscillating at power lines frequency, and oriented along the main neuron axis, can greatly alter the somatic firing activity, with possible functional consequences for cognitive functions.…”

“…Different morphologies, for example without basal dendrites (as in Berzhanskaya et al .) will behave in different ways, as we have shown for stylized neurons in our previous paper (Cavarretta et al ., ).…”

“…Migliore, ; Marcelin et al ., ; Ascoli et al ., ; Migliore et al ., ). The effects of externally applied electric fields were modeled as in Cavarretta et al ., using the NEURON extracellular mechanism (schematically illustrated in Fig. S1).…”

“…This is well within the frequency range of the gamma rhythm, which organizes neuronal activity in time and is currently considered to play a critical role in cognitive functions. Using biophysically and morphologically accurate hippocampal CA1 pyramidal neurons, validated against experimental findings, we have recently shown (Cavarretta et al ., ) how individual neuronal morphology, ion channel dendritic distribution and orientation relative to the field can contribute to the overall effect observed at the cellular level. These results provided a physiological rationale for inconsistent experimental findings, as well as new data and experimentally testable predictions regarding neural effects of power line emissions.…”